Mechanical regulation of cardiac development

Frontiers in Physiology

Volumn 5 AUG, Issue , 2014, Pages

  Lindsey, Stephanie E ^a   Butcher, Jonathan T ^a   Yalcin, Huseyin C ^b  

^a Cornell University   (United States)

^b DOGUS UNIVERSITY   (Turkey)

Author keywords

Congenital heart defects; Heart development; Hemodynamics; Mechanotransduction; Shear stress

Indexed keywords

CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONGENITAL HEART MALFORMATION; CORONARY ARTERY BLOOD FLOW; DIASTOLIC BLOOD PRESSURE; EXTRACELLULAR MATRIX; GREAT BLOOD VESSEL; HEART BEAT; HEART CONTRACTION; HEART DEVELOPMENT; HEART HEMODYNAMICS; HEART VALVE; HUMAN; MECHANOTRANSDUCTION; NONHUMAN; REVIEW; SYSTOLIC BLOOD PRESSURE;

EID: 84906495206     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00318     Document Type: Review

References (148)

1. Aleksandrova, A., Czirok, A., Szabo, A., Filla, M. B., Hossain, M. J., Whelan, P. F., et al. (2012). Convective tissue movements play a major role in avian endocardial morphogenesis. Dev. Biol. 363, 348-361. doi: 10.1016/j.ydbio.2011.12.036
2. Auman, H. J., Coleman, H., Riley, H. E., Olale, F., Tsai, H. J., and Yelon, D. (2007). Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 5:e53. doi: 10.1371/journal.pbio.0050053
3. Bartman, T., and Hove, J. (2005). Mechanics and function in heart morphogenesis. Dev. Dyn. 233, 373-381. doi: 10.1002/dvdy.20367
4. Bartman, T., Walsh, E. C., Wen, K. K., McKane, M., Ren, J., Alexander, J., et al. (2004). Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol. 2:E129. doi: 10.1371/journal.pbio.0020129
5. Bauer, M., Siniawski, H., Pasic, M., Schaumann, B., and Hetzer, R. (2006). Different hemodynamic stress of the ascending aorta wall in patients with bicuspid and tricuspid aortic valve. J. Card. Surg. 21, 218-220. doi: 10.1111/j.1540-8191.2006.00219.x
6. Bharadwaj, K. N., Spitz, C., Shekhar, A., Yalcin, H. C., and Butcher, J. T. (2012). Computational fluid dynamics of developing avian outflow tract heart valves. Ann. Biomed. Eng. 40, 2212-2227. doi: 10.1007/s10439-012-0574-8
7. Biechler, S. V., Potts, J. D., Yost, M. J., Junor, L., Goodwin, R. L., and Weidner, J. W. (2010). Mathematical modeling of flow-generated forces in an in vitro system of cardiac valve development. Ann. Biomed. Eng. 38, 109-117. doi: 10.1007/s10439-009-9824-9
8. Bissell, M. M., Hess, A. T., Biasiolli, L., Glaze, S. J., Loudon, M., Pitcher, A., et al. (2013). Aortic dilation in bicuspid aortic valve disease: flow pattern is a major contributor and differs with valve fusion type. Circ. Cardiovasc. Imaging 6, 499-507. doi: 10.1161/CIRCIMAGING.113.000528
9. Bruneau, B. G. (2008). The developmental genetics of congenital heart disease. Nature 451, 943-948. doi: 10.1038/nature06801
10. Burggren, W., Khorrami, S., Pinder, A., and Sun, T. (2004). Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3-4 chicken embryos. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1399-R1406. doi: 10.1152/ajpregu.00086.2004
11. Burggren, W. W. (2004). What is the purpose of the embryonic heart beat? or how facts can ultimately prevail over physiological dogma. Physiol. Biochem. Zool. 77, 333-345. doi: 10.1086/422230
12. Buskohl, P. R., Gould, R. A., and Butcher, J. T. (2012a). Quantification of embryonic atrioventricular valve biomechanics during morphogenesis. J. Biomech. 45, 895-902. doi: 10.1016/j.jbiomech.2011.11.032
13. Buskohl, P. R., Jenkins, J. T., and Butcher, J. T. (2012b). Computational simulation of hemodynamic-driven growth and remodeling of embryonic atrioventricular valves. Biomech. Model. Mechanobiol. 11, 1205-1217. doi: 10.1007/s10237-012-0424-5
14. Butcher, J. T., and Markwald, R. R. (2007). Valvulogenesis: the moving target. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1489-1503. doi: 10.1098/rstb.2007.2130
15. Butcher, J. T., McQuinn, T. C., Sedmera, D., Turner, D., and Markwald, R. R. (2007). Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ. Res. 100, 1503-1511. doi: 10.1161/CIRCRESAHA.107.148684
16. Butcher, J. T., and Nerem, R. M. (2007). Valvular endothelial cells and the mechanoregulation of valvular pathology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1445-1457. doi: 10.1098/rstb.2007.2127
17. Buxboim, A., Ivanovska, I. L., and Discher, D. E. (2010). Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells "feel" outside and in? J. Cell Sci. 123, 297-308. doi: 10.1242/jcs.041186
18. Camenisch, T. D., Molin, D. G. M., Person, A., Runyan, R. B., Gittenberger-de Groot, A. C., McDonald, J. A., et al. (2002). Temporal and distinct TGFß ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev. Biol. 248, 170-181. doi: 10.1006/dbio.2002.0731
19. Chandra, S., Rajamannan, N. M., and Sucosky, P. (2012). Computational assessment of bicuspid aortic valve wall-shear stress: implications for calcific aortic valve disease. Biomech. Model. Mechanobiol. 11, 1085-1096. doi: 10.1007/s10237-012-0375-x
20. Chang, C. (1932). On the reaction of the endocardium to the blood stream in the embryonic heart, with special reference to the endocardial thickenings in the atrioventricular canal and the bulbus cordis. Anat. Rec. 51, 253-265. doi: 10.1002/ar.1090510305
21. Chi, N. C., Bussen, M., Brand-Arzamendi, K., Ding, C., Olgin, J. E., Shaw, R. M., et al. (2010). Cardiac conduction is required to preserve cardiac chamber morphology. Proc. Natl. Acad. Sci. U.S.A. 107, 14662-14667. doi: 10.1073/pnas.0909432107
22. Chiu, Y. N., Norris, R. A., Mahler, G., Recknagel, A., and Butcher, J. T. (2010). Transforming growth factor beta, bone morphogenetic protein, and vascular endothelial growth factor mediate phenotype maturation and tissue remodeling by embryonic valve progenitor cells: relevance for heart valve tissue engineering. Tissue Eng. Part A 16, 3375-3383. doi: 10.1089/ten.tea.2010.0027
23. Chuck, E. T., Freeman, D. M., Watanabe, M., and Rosenbaum, D. S. (1997). Changing activation sequence in the embryonic chick heart. implications for the development of the his-purkinje system. Circ. Res. 81, 470-476. doi: 10.1161/01.RES.81.4.470
24. Cirotto, C., and Arangi, I. (1989). How do avian embryos breathe? oxygen transport in the blood of early chick embryos. Comp. Biochem. Physiol. A Comp. Physiol. 94, 607-613.
25. Clark, E. B., Hu, N., Dummett, J. L., Vandekieft, G. K., Olson, C., and Tomanek, R. (1986). Ventricular function and morphology in chick embryo from stages 18 to 29. Am. J. Physiol. 250, H407-H413.
26. Clark, E. B., Hu, N., and Rosenquist, G. C. (1984). Effect of conotruncal constriction on aortic-mitral valve continuity in the stage 18, 21 and 24 chick embryo. Am. J. Cardiol. 53, 324-327. doi: 10.1016/0002-9149(84)90447-8
27. Combs, M. D., and Yutzey, K. E. (2009). Heart valve development: regulatory networks in development and disease. Circ. Res. 105, 408-421. doi: 10.1161/CIRCRESAHA.109.201566
28. Damon, B. J., Remond, M. C., Bigelow, M. R., Trusk, T. C., Xie, W., Perucchio, R., et al. (2009). Patterns of muscular strain in the embryonic heart wall. Dev. Dyn. 238, 1535-1546. doi: 10.1002/dvdy.21958
29. deAlmeida, A., McQuinn, T., and Sedmera, D. (2007). Increased ventricular preload is compensated by myocyte proliferation in normal and hypoplastic fetal chick left ventricle. Circ. Res. 100, 1363-1370. doi: 10.1161/01.RES.0000266606.88463.cb
30. deAlmedia, A., and Sedmera, D. (2009). Fibroblast growth factor-2 regulates proliferation of cardiac myocytes in normal and hypoplastic left ventricles in the developing chick. Cardiol. Young 19, 159-169. doi: 10.1017/S1047951109003552
31. de Lange, F. J., Moorman, A. F., Anderson, R. H., Manner, J., Soufan, A. T., de Gier-de Vries, C., et al. (2004). Lineage and morphogenetic analysis of the cardiac valves. Circ. Res. 95, 645-654. doi: 10.1161/01.RES.0000141429.13560.cb
32. Dyer, L. A., and Kirby, M. L. (2009). The role of secondary heart field in cardiac development. Dev. Biol. 336, 137-144. doi: 10.1016/j.ydbio.2009.10.009
33. Eisenberg, L. M., and Markwald, R. R. (1995). Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ. Res. 77, 1-6. doi: 10.1161/01.RES.77.1.1
34. Engler, A. J., Carag-Krieger, C., Johnson, C. P., Raab, M., Tang, H. Y., Speicher, D. W., et al. (2008). Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121, 3794-3802. doi: 10.1242/jcs.029678
35. Ettensohn, C. A. (1985). Mechanisms of epithelial invagination. Q. Rev. Biol. 60, 289-307. doi: 10.1086/414426
36. Fahed, A. C., Gelb, B. D., Seidman, J. G., and Seidman, C. E. (2013). Genetics of congenital heart disease: the glass half empty. Circ. Res. 112, 707-720. doi: 10.1161/CIRCRESAHA.112.300853
37. Forouhar, A. S., Liebling, M., Hickerson, A., Nasiraei-Moghaddam, A., Tsai, H. J., Hove, J. R., et al. (2006). The embryonic vertebrate heart tube is a dynamic suction pump. Science 312, 751-753. doi: 10.1126/science.1123775
38. Garcia-Martinez, V., Sanchez-Quintana, D., and Hurle, J. M. (1991). Histochemical and ultrastructural changes in the extracellular matrix of the developing chick semilunar heart valves. Acta Anat. 142, 87-96. doi: 10.1159/000147166
39. Gjorevski, N., and Nelson, C. M. (2010). The mechanics of development: models and methods for tissue morphogenesis. Birth Defects Res. C Embryo Today 90, 193-202. doi: 10.1002/bdrc.20185
40. Goenezen, S., Rennie, M. Y., and Rugonyi, S. (2012). Biomechanics of early cardiac development. Biomech. Model. Mechanobiol. 11, 1187-1204. doi: 10.1007/s10237-012-0414-7
41. Gourdie, R. G., Harris, B. S., Bond, J., Justus, C., Hewett, K. W., O'Brien, T. X., et al. (2003). Development of the cardiac pacemaking and conduction system. Birth Defects Res. C Embryo Today 69, 46-57. doi: 10.1002/bdrc.10008
42. Granados-Riveron, J. T., and Brook, J. D. (2012). The impact of mechanical forces in heart morphogenesis. Circ. Cardiovasc. Genet. 5, 132-142. doi: 10.1161/CIRCGENETICS.111.961086
43. Groenendijk, B. C., Hierck, B. P., Gittenberger-De Groot, A. C., and Poelmann, R. E. (2004). Development-related changes in the expression of shear stress responsive genes KLF-2, ET-1, and NOS-3 in the developing cardiovascular system of chicken embryos. Dev. Dyn. 230, 57-68. doi: 10.1002/dvdy.20029
44. Groenendijk, B. C., Hierck, B. P., Vrolijk, J., Baiker, M., Pourquie, M. J., Gittenberger-de Groot, A. C., et al. (2005). Changes in shear stress-related gene expression after experimentally altered venous return in the chicken embryo. Circ. Res. 96, 1291-1298. doi: 10.1161/01.RES.0000171901.40952.0d
45. Hadjipanayi, E., Mudera, V., and Brown, R. A. (2009). Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness. J. Tissue Eng. Regen. Med. 3, 77-84. doi: 10.1002/term.136
46. Harh, J. Y., Paul, M. H., Gallen, W. J., Friedberg, D. Z., and Kaplan, S. (1973). Experimental production of hypoplastic left heart syndrome in the chick embryo. Am. J. Cardiol. 31, 51-56. doi: 10.1016/0002-9149(73)90810-2
47. Hickerson, A., Rinderknecht, D., and Gharib, M. (2005). Experimental behavior of a valveless impedance pump. Exp. Fluids 38, 534-540. doi: 10.1007/s00348-005-0946-z
48. Hierck, B. P., Van der Heiden, K., Poelma, C., Westerweel, J., and Poelmann, R. E. (2008). Fluid shear stress and inner curvature remodeling of the embryonic heart. choosing the right lane. Scientific World Journal 8, 212-222. doi: 10.1100/tsw.2008.42
49. Hogers, B., DeRuiter, M. C., Baasten, A. M., Gittenberger-de Groot, A. C., and Poelmann, R. E. (1995). Intracardiac blood flow patterns related to the yolk sac circulation of the chick embryo. Circ. Res. 76, 871-877. doi: 10.1161/01.RES.76.5.871
50. Hogers, B., DeRuiter, M. C., Gittenberger-de Groot, A. C., and Poelmann, R. E. (1997). Unilateral vitelline vein ligation alters intracardiac blood flow patterns and morphogenesis in the chick embryo. Circ. Res. 80, 473-481. doi: 10.1161/01.RES.80.4.473
51. Hogers, B., DeRuiter, M. C., Gittenberger-de Groot, A. C., and Poelmann, R. E. (1999). Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal. Cardiovasc. Res. 41, 87-99. doi: 10.1016/S0008-6363(98)00218-1
52. Hove, J. R., Koster, R. W., Forouhar, A. S., Acevedo-Bolton, G., Fraser, S. E., and Gharib, M. (2003). Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421, 172-177. doi: 10.1038/nature01282
53. Hu, N., Christensen, D. A., Agrawal, A. K., Beaumont, C., Clark, E. B., and Hawkins, J. A. (2009). Dependence of aortic arch morphogenesis on intracardiac blood flow in the left atrial ligated chick embryo. Anat. Rec. 292, 652-660. doi: 10.1002/ar.20885
54. Hu, N., and Clark, E. B. (1989). Hemodynamics of the stage 12 to stage 29 chick embryo. Circ. Res. 65, 1665-1670. doi: 10.1161/01.RES.65.6.1665
55. Huang, J. B., Liu, Y. L., Sun, P. W., Lv, X. D., Du, M., and Fan, X. M. (2010). Molecular mechanisms of congenital heart disease. Cardiovasc. Pathol. 19, e183-e193. doi: 10.1016/j.carpath.2009.06.008
56. Icardo, J. M., and Colvee, E. (1995). Atrioventricular valves of the mouse: III. collagenous skeleton and myotendinous junction. Anat. Rec. 243, 367-375. doi: 10.1002/ar.1092430311
57. Ilbawi, A. M., Spicer, D. E., Bharati, S., Cook, A., and Anderson, R. H. (2007). Morphologic study of the ascending aorta and aortic arch in hypoplastic left hearts: surgical implications. J. Thorac. Cardiovasc. Surg. 134, 99-105. doi: 10.1016/j.jtcvs.2007.01.070
58. Jaffee, O. C. (1965). Hemodynamic factors in the development of the chick embryo heart. Anat. Rec. 151, 69-75. doi: 10.1002/ar.1091510107
59. Johnson, B. M., Garrity, D. M., and Dasi, L. P. (2013). The transitional cardiac pumping mechanics in the embryonic heart. Cardiovasc. Eng. Technol. 4, 246-255. doi: 10.1007/s13239-013-0120-3
60. Kamino, K., Hirota, A., and Fujii, S. (1981). Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature 290, 595-597. doi: 10.1038/290595a0
61. Kowalski, W. J., Dur, O., Wang, Y., Patrick, M. J., Tinney, J. P., Keller, B. B., et al. (2013). Critical transitions in early embryonic aortic arch patterning and hemodynamics. PLoS ONE 8:e60271. doi: 10.1371/journal.pone.0060271
62. Kowalski, W. J., Teslovich, N. C., Menon, P. G., Tinney, J. P., Keller, B. B., and Pekkan, K. (2014). Left atrial ligation alters intracardiac flow patterns and the biomechanical landscape in the chick embryo. Dev. Dyn. 243, 652-662. doi: 10.1002/dvdy.24107
63. Latacha, K. S., Remond, M. C., Ramasubramanian, A., Chen, A. Y., Elson, E. L., and Taber, L. A. (2005). Role of actin polymerization in bending of the early heart tube. Dev. Dyn. 233, 1272-1286. doi: 10.1002/dvdy.20488
64. Liebau, G. (1955). Principles of blood circulation of the heart. Z. Kreislaufforsch. 44, 677-684.
65. Liebau, G. (1956). Possibility of movement of blood in cardiovascular system without cardiac and venous valve function. Verh. Dtsch. Ges. Kreislaufforsch. 22, 354-359.
66. Lin, I. E., and Taber, L. A. (1995). A model for stress-induced growth in the developing heart. J. Biomech. Eng. 117, 343-349. doi: 10.1115/1.2794190
67. Lindsey, S. E., and Butcher, J. T. (2011). The cycle of form and function in cardiac valvulogenesis. Aswan Heart Cent. Sci. Pract Ser. 2, 10. doi: 10.5339/ahcsps.2011.10
68. Liu, J., Bressan, M., Hassel, D., Huisken, J., Staudt, D., Kikuchi, K., et al. (2010). A dual role for ErbB2 signaling in cardiac trabeculation. Development 137, 3867-3875. doi: 10.1242/dev.053736
69. Lockhart, M., Wirrig, E., Phelps, A., and Wessels, A. (2011). Extracellular matrix and heart development. Birth Defects Res. Part A Clin. Mol. Teratol. 91, 535-550. doi: 10.1002/bdra.20810
70. Lorenz, R., Bock, J., Barker, A. J., von Knobelsdorff-Brenkenhoff, F., Wallis, W., Korvink, J. G., et al. (2014). 4D flow magnetic resonance imaging in bicuspid aortic valve disease demonstrates altered distribution of aortic blood flow helicity. Magn. Reson. Med. 71, 1542-1553. doi: 10.1002/mrm.24802
71. Lucitti, J. L., Jones, E. A., Huang, C., Chen, J., Fraser, S. E., and Dickinson, M. E. (2007). Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134, 3317-3326. doi: 10.1242/dev.02883
72. Lucitti, J. L., Tobita, K., and Keller, B. B. (2005). Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo. J. Exp. Biol. 208, 1877-1885. doi: 10.1242/jeb.01574
73. Luna-Zurita, L., Prados, B., Grego-Bessa, J., Luxan, G., del Monte, G., Benguria, A., et al. (2010). Integration of a notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J. Clin. Invest. 120, 3493-3507. doi: 10.1172/JCI42666
74. Majkut, S., Idema, T., Swift, J., Krieger, C., Liu, A., and Discher, D. E. (2013). Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 23, 2434-2439. doi: 10.1016/j.cub.2013.10.057
75. Mammoto, T., and Ingber, D. E. (2010). Mechanical control of tissue and organ development. Development 137, 1407-1420. doi: 10.1242/dev.024166
76. Manasek, F. J., Burnside, M. B., and Waterman, R. E. (1972). Myocardial cell shape changes as a mechanism of embryonic heart looping. Dev. Biol. 29, 349-371. doi: 10.1016/0012-1606(72)90077-2
77. Manner, J. (2004). On rotation, torsion, lateralization, and handedness of the embryonic heart loop: new insights from a simulation model for the heart loop of chick embryos. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 278, 481-492. doi: 10.1002/ar.a.20036
78. Manner, J., Wessel, A., and Yelbuz, T. M. (2010). How does the tubular embryonic heart work? looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube. Dev. Dyn. 239, 1035-1046. doi: 10.1002/dvdy.22265
79. Manning, A., and McLachlan, J. C. (1990). Looping of chick embryo hearts in vitro. J. Anat. 168, 257-263.
80. McBride, K. L., Zender, G. A., Fitzgerald-Butt, S. M., Koehler, D., Menesses-Diaz, A., Fernbach, S., et al. (2009). Linkage analysis of left ventricular outflow tract malformations (aortic valve stenosis, coarctation of the aorta, and hypoplastic left heart syndrome). Eur. J. Hum. Genet. 17, 811-819. doi: 10.1038/ejhg.2008.255
81. Meilhac, S. M., Esner, M., Kelly, R. G., Nicolas, J. F., and Buckingham, M. E. (2004). The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell 6, 685-698. doi: 10.1016/S1534-5807(04)00133-9
82. Miller, C. E., Wong, C. L., and Sedmera, D. (2003). Pressure overload alters stress-strain properties of the developing chick heart. Am. J. Physiol. Heart Circ. Physiol. 285, H1849-H1856. doi: 10.1152/ajpheart.00384.2002
83. Mironov, V., Visconti, R. P., and Markwald, R. R. (2005). On the role of shear stress in cardiogenesis. Endothelium 12, 259-261. doi: 10.1080/10623320500476708
84. Moorman, A. F., and Christoffels, V. M. (2003). Cardiac chamber formation: development, genes, and evolution. Physiol. Rev. 83, 1223-1267. doi: 10.1152/physrev.00006.2003
85. Moorman, A. F. M., Soufan, A. T., Hagoort, J., De Boer, P. A. J., and Christoffels, V. M. (2004). Development of the building plan of the heart. Ann. N.Y. Acad. Sci. 1015, 171-181. doi: 10.1196/annals.1302.014
86. Natowicz, M., Chatten, J., Clancy, R., Conard, K., Glauser, T., Huff, D., et al. (1988). Genetic disorders and major extracardiac anomalies associated with the hypoplastic left heart syndrome. Pediatrics 82, 698-706.
87. Nemer, M. (2008). Genetic insights into normal and abnormal heart development. Cardiovasc. Pathol. 17, 48-54. doi: 10.1016/j.carpath.2007.06.005
88. Nerurkar, N. L., Ramasubramanian, A., and Taber, L. A. (2006). Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads. Dev. Dyn. 235, 1822-1829. doi: 10.1002/dvdy.20813
89. Nkomo, V. T., Enriquez-Sarano, M., Ammash, N. M., Melton, L. J. 3rd., Bailey, K. R., Desjardins, V., et al. (2003). Bicuspid aortic valve associated with aortic dilatation: a community-based study. Arterioscler. Thromb. Vasc. Biol. 23, 351-356. doi: 10.1161/01.ATV.0000055441.28842.0A
90. Norris, R. A., Kern, C. B., Wessels, A., Moralez, E. I., Markwald, R. R., and Mjaatvedt, C. H. (2004). Identification and detection of the periostin gene in cardiac development. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 281A, 1227-1233. doi: 10.1002/ar.a.20135
91. Ottesen, J. T. (2003). Valveless pumping in a fluid-filled closed elastic tube-system:one-dimensional theory with experimental validation. J. Math. Biol. 46, 309-332. doi: 10.1007/s00285-002-0179-1
92. Oyen, N., Poulsen, G., Boyd, H. A., Wohlfahrt, J., Jensen, P. K., and Melbye, M. (2009). Recurrence of congenital heart defects in families. Circulation 120, 295-301. doi: 10.1161/CIRCULATIONAHA.109.857987
93. Person, A. D., Klewer, S. E., and Runyan, R. B. (2005). Cell biology of cardiac cushion development. Int. Rev. Cytol. 243, 287-335. doi: 10.1016/S0074-7696(05)43005-3
94. Qayyum, S. R., Webb, S., Anderson, R. H., Verbeek, F. J., Brown, N. A., and Richardson, M. K. (2001). Septation and valvar formation in the outflow tract of the embryonic chick heart. Anat. Rec. 264, 273-283. doi: 10.1002/ar.1162
95. Rana, M. S., Christoffels, V. M., and Moorman, A. F. (2013). A molecular and genetic outline of cardiac morphogenesis. Acta Physiol. 207, 588-615. doi: 10.1111/apha.12061
96. Reckova, M., Rosengarten, C., deAlmeida, A., Stanley, C. P., Wessels, A., Gourdie, R. G., et al. (2003). Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ. Res. 93, 77-85. doi: 10.1161/01.RES.0000079488.91342.B7
97. Roberts, W. C. (1970). The congenitally bicuspid aortic valve. A study of 85 autopsy cases. Am. J. Cardiol. 26, 72-83. doi: 10.1016/0002-9149(70)90761-7
98. Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Adams, R. J., Berry, J. D., Brown, T. M., et al. (2011). Heart disease and stroke statistics-2011 update: a report from the american heart association. Circulation 123, e18-e209. doi: 10.1161/CIR.0b013e3182009701
99. Rugonyi, S. (2013). Strain-induced tissue growth laws: applications to embryonic cardiovascular development. J. Appl. Mech. Eng. S11:001. doi: 10.4172/2168-9873.S11-001
100. Rugonyi, S., Shaut, C., Liu, A., Thornburg, K., and Wang, R. K. (2008). Changes in wall motion and blood flow in the outflow tract of chick embryonic hearts observed with optical coherence tomography after outflow tract banding and vitelline-vein ligation. Phys. Med. Biol. 53, 5077-5091. doi: 10.1088/0031-9155/53/18/015
101. Runyan, R. B., and Markwald, R. R. (1983). Invasion of mesenchyme into three-dimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev. Biol. 95, 108-114. doi: 10.1016/0012-1606(83)90010-6
102. Samsa, L. A., Yang, B., and Liu, J. (2013). Embryonic cardiac chamber maturation: trabeculation, conduction, and cardiomyocyte proliferation. Am. J. Med. Genet. C Semin. Med. Genet. 163C, 157-168. doi: 10.1002/ajmg.c.31366
103. Sankova, B., Machalek, J., and Sedmera, D. (2010). Effects of mechanical loading on early conduction system differentiation in the chick. Am. J. Physiol. Heart Circ. Physiol. 298, H1571-H1576. doi: 10.1152/ajpheart.00721.2009
104. Schroeder, J. A., Jackson, L. F., Lee, D. C., and Camenisch, T. D. (2003). Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling. J. Mol. Med. 81, 392-403. doi: 10.1007/s00109-003-0456-5
105. Sedmera, D., Harris, B. S., Grant, E., Zhang, N., Jourdan, J., Kurkova, D., et al. (2008). Cardiac expression patterns of endothelin-converting enzyme (ECE): implications for conduction system development. Dev. Dyn. 237, 1746-1753. doi: 10.1002/dvdy.21572
106. Sedmera, D., Hu, N., Weiss, K. M., Keller, B. B., Denslow, S., and Thompson, R. P. (2002). Cellular changes in experimental left heart hypoplasia. Anat. Rec. 267, 137-145. doi: 10.1002/ar.10098
107. Sedmera, D., Pexieder, T., Rychterova, V., Hu, N., and Clark, E. B. (1999). Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat. Rec. 254, 238-252.
108. Sedmera, D., and Thompson, R. P. (2011). Myocyte proliferation in the developing heart. Dev. Dyn. 240, 1322-1334. doi: 10.1002/dvdy.22650
109. Shiraishi, I., Takamatsu, T., Minamikawa, T., and Fujita, S. (1992). 3-D observation of actin filaments during cardiac myofibrinogenesis in chick embryo using a confocal laser scanning microscope. Anat. Embryol. 185, 401-408. doi: 10.1007/BF00188551
110. Simpson, J. M., and Sharland, G. K. (1997). Natural history and outcome of aortic stenosis diagnosed prenatally. Heart 77, 205-210. doi: 10.1136/hrt.77.3.205
111. Snarr, B. S., Kern, C. B., and Wessels, A. (2008). Origin and fate of cardiac mesenchyme. Dev. Dyn. 237, 2804-2819. doi: 10.1002/dvdy.21725
112. Srivastava, D., and Olson, E. N. (2000). A genetic blueprint for cardiac development. Nature 407, 221-226. doi: 10.1038/35025190
113. Sugi, Y., Ito, N., Szebenyi, G., Myers, K., Fallon, J. F., Mikawa, T., et al. (2003). Fibroblast growth factor (FGF)-4 can induce proliferation of cardiac cushion mesenchymal cells during early valve leaflet formation. Dev. Biol. 258, 252-263. doi: 10.1016/S0012-1606(03)00099-X
114. Taber, L. A. (1998). Mechanical aspects of cardiac development. Prog. Biophys. Mol. Biol. 69, 237-255. doi: 10.1016/S0079-6107(98)00010-8
115. Taber, L. A. (2006). Biophysical mechanisms of cardiac looping. Int. J. Dev. Biol. 50, 323-332. doi: 10.1387/ijdb.052045lt
116. Taber, L. A. (2009). Towards a unified theory for morphomechanics. Philos. Trans. A Math. Phys. Eng. Sci. 367, 3555-3583. doi: 10.1098/rsta.2009.0100
117. Taber, L. A., and Eggers, D. W. (1996). Theoretical study of stress-modulated growth in the aorta. J. Theor. Biol. 180, 343-357. doi: 10.1006/jtbi.1996.0107
118. Taber, L. A., Voronov, D. A., and Ramasubramanian, A. (2010). The role of mechanical forces in the torsional component of cardiac looping. Ann. N.Y. Acad. Sci. 1188, 103-110. doi: 10.1111/j.1749-6632.2009.05089.x
119. Taber, L. A., Zhang, J., and Perucchio, R. (2007). Computational model for the transition from peristaltic to pulsatile flow in the embryonic heart tube. J. Biomech. Eng. 129, 441-449. doi: 10.1115/1.2721076
120. Tan, H., Biechler, S., Junor, L., Yost, M. J., Dean, D., Li, J., et al. (2013). Fluid flow forces and rhoA regulate fibrous development of the atrioventricular valves. Dev. Biol. 374, 345-356. doi: 10.1016/j.ydbio.2012.11.023
121. Tan, H., Junor, L., Price, R. L., Norris, R. A., Potts, J. D., and Goodwin, R. L. (2011). Expression and deposition of fibrous extracellular matrix proteins in cardiac valves during chick development. Microsc. Microanal. 17, 91-100. doi: 10.1017/S1431927610094365
122. Tavares, A. L. P., Mercado-Pimentel, M. E., Runyan, R. B., and Kitten, G. T. (2006). TGF?-mediated RhoA expression is necessary for epithelial-mesenchymal transition in the embryonic chick heart. Dev. Dyn. 235, 1589-1598. doi: 10.1002/dvdy.20771
123. Tobita, K., and Keller, B. B. (2000). Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am. J. Physiol. Heart Circ. Physiol. 279, H959-H969.
124. Tobita, K., Schroder, E. A., Tinney, J. P., Garrison, J. B., and Keller, B. B. (2002). Regional passive ventricular stress-strain relations during development of altered loads in chick embryo. Am. J. Physiol. Heart Circ. Physiol. 282, H2386-H2396. doi: 10.1152/ajpheart.00879.2001
125. van den Berg, G., and Moorman, A. F. (2009). Concepts of cardiac development in retrospect. Pediatr. Cardiol. 30, 580-587. doi: 10.1007/s00246-008-9369-y
126. Varner, V. D., and Taber, L. A. (2012). Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly. Development 139, 1680-1690. doi: 10.1242/dev.073486
127. Vermot, J., Forouhar, A. S., Liebling, M., Wu, D., Plummer, D., Gharib, M., et al. (2009). Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol. 7:e1000246. doi: 10.1371/journal.pbio.1000246
128. Verzi, M. P., McCulley, D. J., De Val, S., Dodou, E., and Black, B. L. (2005). The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 287, 134-145. doi: 10.1016/j.ydbio.2005.08.041
129. Voronov, D. A., Alford, P. W., Xu, G., and Taber, L. A. (2004). The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo. Dev. Biol. 272, 339-350. doi: 10.1016/j.ydbio.2004.04.033
130. Voronov, D. A., and Taber, L. A. (2002). Cardiac looping in experimental conditions: effects of extraembryonic forces. Dev. Dyn. 224, 413-421. doi: 10.1002/dvdy.10121
131. Wang, Y., Dur, O., Patrick, M. J., Tinney, J. P., Tobita, K., Keller, B. B., et al. (2009). Aortic arch morphogenesis and flow modeling in the chick embryo. Ann. Biomed. Eng. 37, 1069-1081. doi: 10.1007/s10439-009-9682-5
132. Wenink, A. C., and Gittenberger-de Groot, A. C. (1986). Embryology of the mitral valve. Int. J. Cardiol. 11, 75-84. doi: 10.1016/0167-5273(86)90201-9
133. Wessels, A., and Sedmera, D. (2003). Developmental anatomy of the heart: a tale of mice and man. Physiol. Genomics 15, 165-176. doi: 10.1152/physiolgenomics.00033.2003
134. Wessels, A., van den Hoff, M. J. B., Adamo, R. F., Phelps, A. L., Lockhart, M. M., Sauls, K., et al. (2012). Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart. Dev. Biol. 366, 111-124. doi: 10.1016/j.ydbio.2012.04.020
135. Winer, J. P., Janmey, P. A., McCormick, M. E., and Funaki, M. (2009). Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng. Part A 15, 147-154. doi: 10.1089/ten.tea.2007.0388
136. Wyczalkowski, M. A., Chen, Z., Filas, B. A., Varner, V. D., and Taber, L. A. (2012). Computational models for mechanics of morphogenesis. Birth Defects Res. C Embryo Today 96, 132-152. doi: 10.1002/bdrc.21013
137. Xavier-Neto, J., Castro, R. A., Sampaio, A. C., Azambuja, A. P., Castillo, H. A., Cravo, R. M., et al. (2007). Parallel avenues in the evolution of hearts and pumping organs. Cell. Mol. Life Sci. 64, 719-734. doi: 10.1007/s00018-007-6524-1
138. Ya, J., van den Hoff, M. J., de Boer, P. A., Tesink-Taekema, S., Franco, D., Moorman, A. F., et al. (1998). Normal development of the outflow tract in the rat. Circ. Res. 82, 464-472. doi: 10.1161/01.RES.82.4.464
139. Yalcin, H. C., Shekhar, A., McQuinn, T. C., and Butcher, J. T. (2011). Hemodynamic patterning of the avian atrioventricular valve. Dev. Dyn. 240, 23-35. doi: 10.1002/dvdy.22512
140. Yalcin, H. C., Shekhar, A., Nishimura, N., Rane, A. A., Schaffer, C. B., and Butcher, J. T. (2010). Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects. Am. J. Physiol. Heart Circ. Physiol. 299, H1728-H1735. doi: 10.1152/ajpheart.00495.2010
141. Yanagisawa, H., Yanagisawa, M., Kapur, R. P., Richardson, J. A., Williams, S. C., Clouthier, D. E., et al. (1998). Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 125, 825-836.
142. Yang, M., Taber, L. A., and Clark, E. B. (1994). A nonliner poroelastic model for the trabecular embryonic heart. J. Biomech. Eng. 116, 213-223. doi: 10.1115/1.2895722
143. Yashiro, K., Shiratori, H., and Hamada, H. (2007). Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450, 285-288. doi: 10.1038/nature06254
144. Yener, N., Oktar, G. L., Erer, D., Yardimci, M. M., and Yener, A. (2002). Bicuspid aortic valve. Ann. Thorac. Cardiovasc. Surg. 8, 264-267.
145. Yuan, S., Zaidi, S., and Brueckner, M. (2013). Congenital heart disease: emerging themes linking genetics and development. Curr. Opin. Genet. Dev. 23, 352-359. doi: 10.1016/j.gde.2013.05.004
146. Zaffran, S., Kelly, R. G., Meilhac, S. M., Buckingham, M. E., and Brown, N. A. (2004). Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95, 261-268. doi: 10.1161/01.RES.0000136815.73623.BE
147. Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J. D., et al. (2013). De novo mutations in histone-modifying genes in congenital heart disease. Nature 498, 220-223. doi: 10.1038/nature12141
148. Zamir, E. A., Czirok, A., Cui, C., Little, C. D., and Rongish, B. J. (2006). Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc. Natl. Acad. Sci. U.S.A. 103, 19806-19811. doi: 10.1073/pnas.0606100103