Mechanical regulation of cardiac development

Lindsey, Stephanie E.

doi:10.3389/fphys.2014.00318

Cited by 159Congenital heart defects researchCellular Mechanics and InteractionsCardiac Fibrosis and Remodeling

Mechanical regulation of cardiac development

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Lindsey, Stephanie E.·2014·Frontiers in Physiology

DOI 10.3389/fphys.2014.00318PMC PMC4140306

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Abstract

Mechanical forces are essential contributors to and unavoidable components of cardiac formation, both inducing and orchestrating local and global molecular and cellular changes. Experimental animal studies have contributed substantially to understanding the mechanobiology of heart development. More recent integration of high-resolution imaging modalities with computational modeling has greatly improved our quantitative understanding of hemodynamic flow in heart development. Merging these latest experimental technologies with molecular and genetic signaling analysis will accelerate our understanding of the relationships integrating mechanical and biological signaling for proper cardiac formation. These advances will likely be essential for clinically translatable guidance for targeted interventions to rescue malforming hearts and/or reconfigure malformed circulations for optimal performance. This review summarizes our current understanding on the levels of mechanical signaling in the heart and their roles in orchestrating cardiac development.

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The vitelline and allantoic vascular beds offer mechanical resistance to blood flow, and their inadequate growth promotes mechanical signals in the heart that result in structural defects.
“These vascular beds offer mechanical resistance to blood flow, and there is increasing evidence that their inadequate growth promotes mechanical signals in the heart that result in structural defects (218, 260, 341, 379).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [341]

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Heart Disease and Stroke Statistics—2011 Update: A Report From the American Heart Association
Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Adams, R. J., Berry, J. D., Brown, T. M., Carnethon, M. R., Dai, S., de Simone, G., Ford, E. S., et al. (2011) · Circulation · doi:10.1161/cir.0b013e3182009701 · Cited by 6,149 · see citing works
Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis
Hove, J. R., Köster, R. W., Forouhar, A. S., Acevedo‐Bolton, G., Fraser, S. E., & Gharib, M. (2003) · Nature · doi:10.1038/nature01282 · Cited by 1,000 · see citing works
De novo mutations in histone-modifying genes in congenital heart disease
Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J. D., Romano-Adesman, A., Bjornson, R. D., Breitbart, R. E., Brown, K. K., et al. (2013) · Nature · doi:10.1038/nature12141 · Cited by 934 · see citing works
The congenitally bicuspid aortic valve
Roberts, W. C. (1970) · The American Journal of Cardiology · doi:10.1016/0002-9149(70)90761-7 · Cited by 925 · see citing works
Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating
Engler, A. J., Krieger, C. C., Johnson, C. P., Raab, M., Tang, H., Speicher, D. W., Sanger, J. W., Sanger, J. M., & Discher, D. E. (2008) · Journal of Cell Science · doi:10.1242/jcs.029678 · Cited by 869 · see citing works
Mechanical control of tissue and organ development
Mammoto, T., & Ingber, D. E. (2010) · Development · doi:10.1242/dev.024166 · Cited by 851 · see citing works
The developmental genetics of congenital heart disease
Bruneau, B. G. (2008) · Nature · doi:10.1038/nature06801 · Cited by 783 · see citing works
Cardiac Chamber Formation: Development, Genes, and Evolution
Moorman, A. F. M., & Christoffels, V. M. (2003) · Physiological Reviews · doi:10.1152/physrev.00006.2003 · Cited by 739 · see citing works
The extracellular matrix: an active or passive player in fibrosis?
Wight, T. N., & Potter‐Perigo, S. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00132.2011 · Cited by 669 · see citing works
Molecular Regulation of Atrioventricular Valvuloseptal Morphogenesis
Eisenberg, L. M., & Markwald, R. R. (1995) · Circulation Research · doi:10.1161/01.res.77.1.1 · Cited by 650 · see citing works
A genetic blueprint for cardiac development
Srivastava, D., & Olson, E. N. (2000) · Nature · doi:10.1038/35025190 · Cited by 632 · see citing works
Genetics of Congenital Heart Disease
Fahed, A. C., Gelb, B. D., Seidman, J. G., & Seidman, C. E. (2013) · Circulation Research · doi:10.1161/circresaha.112.300853 · Cited by 572 · see citing works
The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field
Verzi, M. P., McCulley, D. J., Val, S. D., Dodou, E., & Black, B. L. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.08.041 · Cited by 527 · see citing works
Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene
Yanagisawa, H., Yanagisawa, M., Kapur, R. P., Richardson, J. A., Williams, S. C., Clouthier, D. E., de Wit, D., Emoto, N., & Hammer, R. E. (1998) · Development · doi:10.1242/dev.125.5.825 · Cited by 490 · see citing works
Vascular remodeling of the mouse yolk sac requires hemodynamic force
Lucitti, J. L., Jones, E. A. V., Huang, C., Chen, J., Fraser, S. E., & Dickinson, M. E. (2007) · Development · doi:10.1242/dev.02883 · Cited by 478 · see citing works
GENETICS of congenital heart disease.
(1955) · PubMed · Cited by 472 · see citing works
Heart Valve Development
Combs, M. D., & Yutzey, K. E. (2009) · Circulation Research · doi:10.1161/circresaha.109.201566 · Cited by 456 · see citing works
The Clonal Origin of Myocardial Cells in Different Regions of the Embryonic Mouse Heart
Meilhac, S. M., Ešner, M., Kelly, R. G., Nicolas, J.-F., & BUCKINGHAM, M. E. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00133-9 · Cited by 416 · see citing works
Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells ‘feel’ outside and in?
Buxboim, A., Ivanovska, I. L., & Discher, D. E. (2010) · Journal of Cell Science · doi:10.1242/jcs.041186 · Cited by 401 · see citing works
Lineage and Morphogenetic Analysis of the Cardiac Valves
de Lange, F. J., Moorman, A. F. M., Anderson, R. H., Männer, J., Soufan, A. T., Vries, C. D. G.-D., Schneider, M. D., Webb, S., van den Hoff, M. J. B., & Christoffels, V. M. (2004) · Circulation Research · doi:10.1161/01.res.0000141429.13560.cb · Cited by 385 · see citing works
Recurrence of Congenital Heart Defects in Families
Øyen, N., Poulsen, G., Boyd, H. A., Wohlfahrt, J., Jensen, P. K. A., & Melbye, M. (2009) · Circulation · doi:10.1161/circulationaha.109.857987 · Cited by 380 · see citing works
Aortic Dilation in Bicuspid Aortic Valve Disease
Bissell, M. M., Hess, A. T., Biasiolli, L., et al. (2013) · Circulation Cardiovascular Imaging · doi:10.1161/circimaging.113.000528 · Cited by 380 · see citing works
Right Ventricular Myocardium Derives From the Anterior Heart Field
Zaffran, S., Kelly, R. G., Meilhac, S. M., et al. (2004) · Circulation Research · doi:10.1161/01.res.0000136815.73623.be · Cited by 379 · see citing works
Bone Marrow-Derived Human Mesenchymal Stem Cells Become Quiescent on Soft Substrates but Remain Responsive to Chemical or Mechanical Stimuli
Winer-Jones, J. P., Janmey, P. A., McCormick, M. E., & Funaki, M. (2008) · Tissue Engineering Part A · doi:10.1089/ten.tea.2007.0388 · Cited by 375 · see citing works
Cell Biology of Cardiac Cushion Development
Person, A. D., Klewer, S. E., & Runyan, R. B. (2005) · International review of cytology · doi:10.1016/s0074-7696(05)43005-3 · Cited by 369 · see citing works
Reversing Blood Flows Act through klf2a to Ensure Normal Valvulogenesis in the Developing Heart
Vermot, J., Forouhar, A. S., Liebling, M., Wu, D., Plummer, D., Gharib, M., & Fraser, S. E. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000246 · Cited by 320 · see citing works
Hypoplastic left heart syndrome
Barron, D. J., Kilby, M. D., Davies, B., Wright, J. G., Jones, T. J. J., & Brawn, W. J. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60563-8 · Cited by 309 · see citing works
Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness
Hadjipanayi, E., Mudera, V., & Brown, R. (2008) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.136 · Cited by 306 · see citing works
Functional Modulation of Cardiac Form through Regionally Confined Cell Shape Changes
Auman, H. J., Coleman, H., Riley, H. E., Olale, F., Tsai, H., & Yelon, D. L. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050053 · Cited by 286 · see citing works
Heart disease and stroke.
Jp, B. (1994) · PubMed · Cited by 285 · see citing works
Temporal and Distinct TGFβ Ligand Requirements during Mouse and Avian Endocardial Cushion Morphogenesis
Camenisch, T. D., Molin, D. G. M., Person, A., Runyan, R. B., Gittenberger-de Groot, A. C., McDonald, J. A., & Klewer, S. E. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0731 · Cited by 279 · see citing works
The Embryonic Vertebrate Heart Tube Is a Dynamic Suction Pump
Forouhar, A. S., Liebling, M., Hickerson, A. I., Nasiraei‐Moghaddam, A., Tsai, H., Hove, J. R., Fraser, S. E., Dickinson, M. E., & Gharib, M. (2006) · Science · doi:10.1126/science.1123775 · Cited by 277 · see citing works
Invasion of mesenchyme into three-dimensional collagen gels: A regional and temporal analysis of interaction in embryonic heart tissue
Runyan, R. B., & Markwald, R. R. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90010-6 · Cited by 267 · see citing works
Epicardially derived fibroblasts preferentially contribute to the parietal leaflets of the atrioventricular valves in the murine heart
Wessels, A., van den Hoff, M. J. B., Adamo, R. F., Phelps, A. L., Lockhart, M. M., Sauls, K., Briggs, L. E., Norris, R. A., van Wijk, B., Perez-Pomares, J. M., et al. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.04.020 · Cited by 263 · see citing works
The role of secondary heart field in cardiac development
Dyer, L. A., & Kirby, M. L. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.009 · Cited by 262 · see citing works
Developmental anatomy of the heart: a tale of mice and man
Wessels, A., & Sedmera, D. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00033.2003 · Cited by 260 · see citing works
Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions
Sedmera, D., Pexieder, T., Rychterová, V., Hu, N., & Clark, E. B. (1999) · The Anatomical Record · doi:10.1002/(sici)1097-0185(19990201)254:2 · Cited by 252 · see citing works
A dual role for ErbB2 signaling in cardiac trabeculation
Liu, J., Bressan, M. C., Hassel, D., et al. (2010) · Development · doi:10.1242/dev.053736 · Cited by 251 · see citing works
Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation
Luna‐Zurita, L., Prados, B., Grego‐Bessa, J., Luxán, G., del Monte‐Nieto, G., Benguría, A., Adams, R. H., Pérez-Pomares, J. M., & de la Pompa, J. L. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42666 · Cited by 245 · see citing works
Extracellular matrix and heart development
Lockhart, M. M., Wirrig, E. E., Phelps, A. L., & Wessels, A. (2011) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20810 · Cited by 243 · see citing works
Unilateral Vitelline Vein Ligation Alters Intracardiac Blood Flow Patterns and Morphogenesis in the Chick Embryo
Hogers, B., DeRuiter, M. C., Gittenberger-de Groot, A. C., & Poelmann, R. E. (1997) · Circulation Research · doi:10.1161/01.res.80.4.473 · Cited by 232 · see citing works
Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye
Kamino, K., Hirota, A., & Fujii, S. (1981) · Nature · doi:10.1038/290595a0 · Cited by 225 · see citing works
Early Myocardial Function Affects Endocardial Cushion Development in Zebrafish
Bartman, T., Walsh, E. C., Wen, K., McKane, M., Ren, J., Alexander, J. S., Rubenstein, P. A., & Stainier, D. Y. R. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020129 · Cited by 224 · see citing works
Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch
Yashiro, K., Shiratori, H., & Hamada, H. (2007) · Nature · doi:10.1038/nature06254 · Cited by 218 · see citing works
Hemodynamics of the stage 12 to stage 29 chick embryo.
Hu, N., & Clark, E. B. (1989) · Circulation Research · doi:10.1161/01.res.65.6.1665 · Cited by 214 · see citing works
Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling
Schroeder, J. A., Jackson, L. F., Lee, D. C., & Camenisch, T. D. (2003) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0456-5 · Cited by 207 · see citing works
Heart-Specific Stiffening in Early Embryos Parallels Matrix and Myosin Expression to Optimize Beating
Majkut, S., Idema, T., Swift, J., Krieger, C., Liu, A., & Discher, D. E. (2013) · Current Biology · doi:10.1016/j.cub.2013.10.057 · Cited by 198 · see citing works
Natural history and outcome of aortic stenosis diagnosed prenatally.
Simpson, J. M., & Sharland, G. K. (1997) · Heart · doi:10.1136/hrt.77.3.205 · Cited by 190 · see citing works
Bicuspid Aortic Valve Associated With Aortic Dilatation
Nkomo, V. T., Enriquez-Sarano, M. L., Ammash, N. M., Melton, L. J., Bailey, K. R., Desjardins, V. A., Horn, R. A., & Tajik, A. J. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000055441.28842.0a · Cited by 190 · see citing works
Hemodynamics Is a Key Epigenetic Factor in Development of the Cardiac Conduction System
Rečková, M., Rosengarten, C., deAlmeida, A. C., et al. (2003) · Circulation Research · doi:10.1161/01.res.0000079488.91342.b7 · Cited by 187 · see citing works
Genetic Disorders and Major Extracardiac Anomalies Associated With the Hypoplastic Left Heart Syndrome
Natowicz, M. R., Chatten, J., Clancy, R. R., Conard, K. A., Glauser, T. A., Huff, D. S., Lin, A. E., Norwood, W. I., RORKE, L. B., Uri, A. K., et al. (1988) · PEDIATRICS · doi:10.1542/peds.82.5.698 · Cited by 186 · see citing works
Direct Immunological Detection of Wood Cell Wall Polysaccharides after Microwave-Assisted Ionic Liquid Disruption
Plazanet, I., Zerrouki, R., & Lhernould, S. (2015) · Journal of Glycobiology · doi:10.4172/2168-958x.1000115 · Cited by 184 · see citing works
Embryonic cardiac chamber maturation: Trabeculation, conduction, and cardiomyocyte proliferation
Samsa, L. A., Yang, B., & Liu, J. (2013) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31366 · Cited by 173 · see citing works
Changes in Shear Stress–Related Gene Expression After Experimentally Altered Venous Return in the Chicken Embryo
Groenendijk, B. C. W., Hierck, B. P., Vrolijk, J., Baiker, M., Pourquie, M. J. B. M., Groot, A. C. G., & Poelmann, R. E. (2005) · Circulation Research · doi:10.1161/01.res.0000171901.40952.0d · Cited by 166 · see citing works
Theoretical Study of Stress-Modulated Growth in the Aorta
Taber, L. A., & Eggers, D. W. (1996) · Journal of Theoretical Biology · doi:10.1006/jtbi.1996.0107 · Cited by 158 · see citing works
Valvulogenesis: the moving target
Butcher, J. T., & Markwald, R. R. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2130 · Cited by 156 · see citing works
Extraembryonic venous obstructions lead to cardiovascular malformations and can be embryolethal
Hogers, B. (1999) · Cardiovascular Research · doi:10.1016/s0008-6363(98)00218-1 · Cited by 155 · see citing works
Origin and fate of cardiac mesenchyme
Snarr, B. S., Kern, C. B., & Wessels, A. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21725 · Cited by 153 · see citing works
Experimental production of hypoplastic left heart syndrome in the chick embryo
Harh, J. Y., Paul, M. H., Gallen, W. J., Friedberg, D. Z., & Kaplan, S. A. (1973) · The American Journal of Cardiology · doi:10.1016/0002-9149(73)90810-2 · Cited by 150 · see citing works
Transitions in Early Embryonic Atrioventricular Valvular Function Correspond With Changes in Cushion Biomechanics That Are Predictable by Tissue Composition
Butcher, J. T., McQuinn, T. C., Sedmera, D., Turner, D., & Markwald, R. R. (2007) · Circulation Research · doi:10.1161/circresaha.107.148684 · Cited by 147 · see citing works
Valvular endothelial cells and the mechanoregulation of valvular pathology
Butcher, J. T., & Nerem, R. M. (2007) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2127 · Cited by 145 · see citing works
Genetic insights into normal and abnormal heart development
Nemer, M. (2007) · Cardiovascular Pathology · doi:10.1016/j.carpath.2007.06.005 · Cited by 140 · see citing works
Mechanisms of Epithelial Invagination
Ettensohn, C. A. (1985) · The Quarterly Review of Biology · doi:10.1086/414426 · Cited by 139 · see citing works
Normal Development of the Outflow Tract in the Rat
Ya, J., van den Hoff, M. J. B., de Boer, P. A. J., et al. (1998) · Circulation Research · doi:10.1161/01.res.82.4.464 · Cited by 138 · see citing works
Increased Ventricular Preload Is Compensated by Myocyte Proliferation in Normal and Hypoplastic Fetal Chick Left Ventricle
deAlmeida, A. C., McQuinn, T., & Sedmera, D. (2007) · Circulation Research · doi:10.1161/01.res.0000266606.88463.cb · Cited by 137 · see citing works
4D flow magnetic resonance imaging in bicuspid aortic valve disease demonstrates altered distribution of aortic blood flow helicity
Lorenz, R., Bock, J., Barker, A. J., von Knobelsdorff‐Brenkenhoff, F., Wallis, W., Korvink, J. G., Bissell, M. M., Schulz‐Menger, J., & Markl, M. (2013) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24802 · Cited by 132 · see citing works
Computational assessment of bicuspid aortic valve wall-shear stress: implications for calcific aortic valve disease
Chandra, S., Rajamannan, N. M., & Sucosky, P. (2012) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-012-0375-x · Cited by 127 · see citing works
Cellular changes in experimental left heart hypoplasia
Sedmera, D., Hu, N., Weiss, K. M., et al. (2002) · The Anatomical Record · doi:10.1002/ar.10098 · Cited by 126 · see citing works
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
Groenendijk, B. C. W., Hierck, B. P., Groot, A. C. G., & Poelmann, R. E. (2004) · Developmental Dynamics · doi:10.1002/dvdy.20029 · Cited by 126 · see citing works
Myocardial cell shape change as a mechanism of embryonic heart looping
Manasek, F. J., Burnside, M. B., & Waterman, R. E. (1972) · Developmental Biology · doi:10.1016/0012-1606(72)90077-2 · Cited by 120 · see citing works
The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo
Voronov, D. A., Alford, P. W., Xu, G., & Taber, L. A. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2004.04.033 · Cited by 120 · see citing works
Biophysical mechanisms of cardiac looping
Taber, L. A. (2006) · The International Journal of Developmental Biology · doi:10.1387/ijdb.052045lt · Cited by 111 · see citing works
Development of the cardiac pacemaking and conduction system
Gourdie, R. G., Harris, B. S., Bond, J. S., Justus, C. D., Hewett, K. W., O’Brien, T. X., Thompson, R. P., & Sedmera, D. (2003) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.10008 · Cited by 110 · see citing works
Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos
Tobita, K., & Keller, B. B. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.3.h959 · Cited by 108 · see citing works
Towards a unified theory for morphomechanics
Taber, L. A. (2009) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2009.0100 · Cited by 107 · see citing works
Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements
Zamir, E. A., Czirók, A., Cui, C., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606100103 · Cited by 105 · see citing works
How does the tubular embryonic heart work? Looking for the physical mechanism generating unidirectional blood flow in the valveless embryonic heart tube
Männer, J., Wessel, A., & Yelbuz, T. M. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22265 · Cited by 104 · see citing works
Cardiac conduction is required to preserve cardiac chamber morphology
Chi, N. C., Bussen, M., Brand‐Arzamendi, K., Ding, C., Olgin, J. E., Shaw, R. M., Martin, G. R., & Stainier, D. Y. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909432107 · Cited by 104 · see citing works
Changing Activation Sequence in the Embryonic Chick Heart
Chuck, E. T., Freeman, D. M., Watanabe, M., et al. (1997) · Circulation Research · doi:10.1161/01.res.81.4.470 · Cited by 102 · see citing works
A molecular and genetic outline of cardiac morphogenesis
Rana, M. S., Christoffels, V. M., & Moorman, A. F. M. (2013) · Acta Physiologica · doi:10.1111/apha.12061 · Cited by 100 · see citing works
What Is the Purpose of the Embryonic Heart Beat? or How Facts Can Ultimately Prevail over Physiological Dogma
Burggren, W. W. (2004) · Physiological and Biochemical Zoology · doi:10.1086/422230 · Cited by 97 · see citing works
Myocyte proliferation in the developing heart
Sedmera, D., & Thompson, R. P. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22650 · Cited by 96 · see citing works
Biomechanics of early cardiac development
Goenezen, S., Rennie, M. Y., & Rugonyi, S. (2012) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-012-0414-7 · Cited by 94 · see citing works
Experimental study of the behavior of a valveless impedance pump
Hickerson, A. I., Rinderknecht, D. G., & Gharib, M. (2005) · Experiments in Fluids · doi:10.1007/s00348-005-0946-z · Cited by 94 · see citing works
Cardiac looping in experimental conditions: Effects of extraembryonic forces
Voronov, D. A., & Taber, L. A. (2002) · Developmental Dynamics · doi:10.1002/dvdy.10121 · Cited by 91 · see citing works
Mechanical aspects of cardiac development
Taber, L. A. (1998) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(98)00010-8 · Cited by 91 · see citing works
Linkage analysis of left ventricular outflow tract malformations (aortic valve stenosis, coarctation of the aorta, and hypoplastic left heart syndrome)
McBride, K. L., Zender, G. A., Fitzgerald‐Butt, S. M., et al. (2009) · European Journal of Human Genetics · doi:10.1038/ejhg.2008.255 · Cited by 91 · see citing works
Valveless pumping in a fluid-filled closed elastic tube-system: one-dimensional theory with experimental validation
Ottesen, J. T. (2003) · Journal of Mathematical Biology · doi:10.1007/s00285-002-0179-1 · Cited by 90 · see citing works
Computational models for mechanics of morphogenesis
Wyczalkowski, M. A., Chen, Z., Filas, B. A., Varner, V. D., & Taber, L. A. (2012) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21013 · Cited by 90 · see citing works
The Impact of Mechanical Forces in Heart Morphogenesis
Granados-Riveron, J. T., & Brook, J. D. (2012) · Circulation: Cardiovascular Genetics · doi:10.1161/circgenetics.111.961086 · Cited by 90 · see citing works
Aortic Arch Morphogenesis and Flow Modeling in the Chick Embryo
Wang, Y., Dur, O., Patrick, M. J., Tinney, J. P., Tobita, K., Keller, B. B., & Pekkan, K. (2009) · Annals of Biomedical Engineering · doi:10.1007/s10439-009-9682-5 · Cited by 89 · see citing works
Mechanics and function in heart morphogenesis
Bartman, T., & Hove, J. R. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20367 · Cited by 88 · see citing works
A Model for Stress-Induced Growth in the Developing Heart
Lin, I.-E., & Taber, L. A. (1995) · Journal of Biomechanical Engineering · doi:10.1115/1.2794190 · Cited by 83 · see citing works
Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly
Varner, V. D., & Taber, L. A. (2012) · Development · doi:10.1242/dev.073486 · Cited by 83 · see citing works
Intracardiac Blood Flow Patterns Related to the Yolk Sac Circulation of the Chick Embryo
Hogers, B., DeRuiter, M. C., Baasten, A. M. J., Groot, A. C. G., & Poelmann, R. E. (1995) · Circulation Research · doi:10.1161/01.res.76.5.871 · Cited by 83 · see citing works
Fibroblast growth factor (FGF)-4 can induce proliferation of cardiac cushion mesenchymal cells during early valve leaflet formation
Sugi, Y., Ito, N., Szebenyi, G., Myers, K., Fallon, J. F., Mikawa, T., & Markwald, R. R. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00099-x · Cited by 80 · see citing works
Hemodynamic factors in the development of the chick embryo heart
Jaffee, O. C. (1965) · The Anatomical Record · doi:10.1002/ar.1091510107 · Cited by 79 · see citing works
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
Rugonyi, S., Shaut, C., Liu, A., Thornburg, K. L. R., & Wang, R. K. (2008) · Physics in Medicine and Biology · doi:10.1088/0031-9155/53/18/015 · Cited by 78 · see citing works
Regional passive ventricular stress-strain relations during development of altered loads in chick embryo
Tobita, K., Schroder, E. A., Tinney, J. P., et al. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00879.2001 · Cited by 77 · see citing works
TGFβ‐mediated RhoA expression is necessary for epithelial‐mesenchymal transition in the embryonic chick heart
Tavares, A. L. P., Mercado-Pimentel, M. E., Runyan, R. B., & Kitten, G. T. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20771 · Cited by 76 · see citing works
Role of actin polymerization in bending of the early heart tube
Latacha, K. S., Rémond, M. C., Ramasubramanian, A., et al. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20488 · Cited by 73 · see citing works
Experimental study of the behavior of a valveless impedance pump
Hickerson, A. I., Rinderknecht, D. G., & Gharib, M. (2005) · Experiments in Fluids · doi:10.1007/s00348-005-0029-1 · Cited by 72 · see citing works
Hemodynamic patterning of the avian atrioventricular valve
Yalcin, H. C., Shekhar, A., McQuinn, T. C., & Butcher, J. T. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22512 · Cited by 72 · see citing works
Ventricular function and morphology in chick embryo from stages 18 to 29
Clark, E. B., Hu, N., Dummett, J. L., et al. (1986) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1986.250.3.h407 · Cited by 71 · see citing works
Different Hemodynamic Stress of the Ascending Aorta Wall in Patients with Bicuspid and Tricuspid Aortic Valve
Bauer, M. F., Siniawski, H., Pašić, M., et al. (2006) · Journal of Cardiac Surgery · doi:10.1111/j.1540-8191.2006.00219.x · Cited by 71 · see citing works
Identification and detection of the periostin gene in cardiac development
Norris, R. A., Kern, C. B., Wessels, A., et al. (2004) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20135 · Cited by 71 · see citing works
On rotation, torsion, lateralization, and handedness of the embryonic heart loop: New insights from a simulation model for the heart loop of chick embryos
Männer, J. (2004) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20036 · Cited by 70 · see citing works
The mechanics of development: Models and methods for tissue morphogenesis
Gjorevski, N., & Nelson, C. M. (2010) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20185 · Cited by 67 · see citing works
Bicuspid aortic valve.
Yener, N., Oktar, G. L., Erer, D., et al. (2002) · PubMed · Cited by 67 · see citing works
Molecular mechanisms of congenital heart disease
Huang, J.-B., Liu, Y., Pei-wu, S., et al. (2009) · Cardiovascular Pathology · doi:10.1016/j.carpath.2009.06.008 · Cited by 65 · see citing works
Congenital heart disease: emerging themes linking genetics and development
Yuan, S., Zaidi, S., & Brueckner, M. (2013) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.05.004 · Cited by 64 · see citing works
Septation and valvar formation in the outflow tract of the embryonic chick heart
Qayyum, S. R., Webb, S., Anderson, R. H., Verbeek, F. J., Brown, N. A., & Richardson, M. K. (2001) · The Anatomical Record · doi:10.1002/ar.1162 · Cited by 61 · see citing works
3-D observation of actin filaments during cardiac myofibrinogenesis in chick embryo using a confocal laser scanning microscope
Shiraishi, I., Takamatsu, T., Minamikawa, T., et al. (1992) · Anatomy and Embryology · doi:10.1007/bf00188551 · Cited by 60 · see citing works
Looping of chick embryo hearts in vitro.
Manning, A., & McLachlan, J. C. (1990) · PubMed · Cited by 59 · see citing works
Fluid Shear Stress and Inner Curvature Remodeling of the Embryonic Heart. Choosing the Right Lane!
Hierck, B. P., der Heiden, K. V., Poelma, C., Westerweel, J., & Poelmann, R. E. (2008) · The Scientific World JOURNAL · doi:10.1100/tsw.2008.42 · Cited by 59 · see citing works
Arterial hemodynamics and mechanical properties after circulatory intervention in the chick embryo
Lucitti, J. L., Tobita, K., & Keller, B. B. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01574 · Cited by 59 · see citing works
Dependence of Aortic Arch Morphogenesis on Intracardiac Blood Flow in the Left Atrial Ligated Chick Embryo
Hu, N., Christensen, D. A., Agrawal, A., et al. (2009) · The Anatomical Record · doi:10.1002/ar.20885 · Cited by 57 · see citing works
Computational Model for the Transition From Peristaltic to Pulsatile Flow in the Embryonic Heart Tube
Taber, L. A., Zhang, J., & Perucchio, R. (2006) · Journal of Biomechanical Engineering · doi:10.1115/1.2721076 · Cited by 55 · see citing works
Effect of conotruncal constriction on aortic-mitral valve continuity in the stage 18, 21 and 24 chick embryo
Clark, E. B., Hu, N., & Rosenquist, G. C. (1984) · The American Journal of Cardiology · doi:10.1016/0002-9149(84)90447-8 · Cited by 52 · see citing works
Critical Transitions in Early Embryonic Aortic Arch Patterning and Hemodynamics
Kowalski, W. J., Dur, O., Wang, Y., Patrick, M. J., Tinney, J. P., Keller, B. B., & Pekkan, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060271 · Cited by 50 · see citing works
Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads
Nerurkar, N. L., Ramasubramanian, A., & Taber, L. A. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20813 · Cited by 50 · see citing works
Pressure overload alters stress-strain properties of the developing chick heart
Miller, C. E., Wong, C. L., & Sedmera, D. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00384.2002 · Cited by 49 · see citing works
A Nonliner Poroelastic Model for the Trabecular Embryonic Heart
Yang, M. “., Taber, L. A., & Clark, E. B. (1994) · Journal of Biomechanical Engineering · doi:10.1115/1.2895722 · Cited by 48 · see citing works
Development of the Building Plan of the Heart
Moorman, A., Soufan, A., Hagoort, J., Boer, P. A. J., & Christoffels, V. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1302.014 · Cited by 48 · see citing works
Convective tissue movements play a major role in avian endocardial morphogenesis
Aleksandrova, A., Czirók, A., Szabó, A., Filla, M. B., Hossain, M. J., Whelan, P. F., Lansford, R. D., & Rongish, B. J. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2011.12.036 · Cited by 48 · see citing works
The role of mechanical forces in the torsional component of cardiac looping
Taber, L. A., Voronov, D. A., & Ramasubramanian, A. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05089.x · Cited by 45 · see citing works
Fluid flow forces and rhoA regulate fibrous development of the atrioventricular valves
Tan, H., Biechler, S. V., Junor, L., Yost, M. J., Dean, D. M. D., Li, J., Potts, J. D., & Goodwin, R. L. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.11.023 · Cited by 44 · see citing works
Atrioventricular valves of the mouse: III. Collagenous skeleton and myotendinous junction
Icardo, J. M., & Colvée, E. (1995) · The Anatomical Record · doi:10.1002/ar.1092430311 · Cited by 43 · see citing works
Concepts of Cardiac Development in Retrospect
van den Berg, G., & Moorman, A. F. M. (2009) · Pediatric Cardiology · doi:10.1007/s00246-008-9369-y · Cited by 42 · see citing works
Embryology of the mitral valve
Wenink, A. C. G., & Groot, A. C. G. (1986) · International Journal of Cardiology · doi:10.1016/0167-5273(86)90201-9 · Cited by 41 · see citing works
Computational Fluid Dynamics of Developing Avian Outflow Tract Heart Valves
Bharadwaj, K. N., Spitz, C., Shekhar, A., Yalcin, H. C., & Butcher, J. T. (2012) · Annals of Biomedical Engineering · doi:10.1007/s10439-012-0574-8 · Cited by 41 · see citing works
Cardiovascular development: towards biomedical applicability
Xavier‐Neto, J., Castro, R. A., Sampaio, A. C., Azambujá, A. P., Castillo, H. A., Cravo, R. M., & Simões-Costa, M. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6524-1 · Cited by 40 · see citing works
Two-photon microscopy-guided femtosecond-laser photoablation of avian cardiogenesis: noninvasive creation of localized heart defects
Yalcin, H. C., Shekhar, A., Nishimura, N., et al. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00495.2010 · Cited by 37 · see citing works
Left atrial ligation alters intracardiac flow patterns and the biomechanical landscape in the chick embryo
Kowalski, W. J., Teslovich, N. C., Menon, P. G., Tinney, J. P., Keller, B. B., & Pekkan, K. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24107 · Cited by 36 · see citing works
Transforming Growth Factor β, 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
Chiu, Y.-N., Norris, R. A., Mahler, G. J., Recknagel, A. K., & Butcher, J. T. (2010) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0027 · Cited by 34 · see citing works
Quantification of embryonic atrioventricular valve biomechanics during morphogenesis
Buskohl, P. R., Gould, R. A., & Butcher, J. T. (2011) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2011.11.032 · Cited by 32 · see citing works
Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3–4 chicken embryos
Burggren, W. W., Khorrami, S., Pinder, A. W., & Sun, T. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00086.2004 · Cited by 32 · see citing works
Computational simulation of hemodynamic-driven growth and remodeling of embryonic atrioventricular valves
Buskohl, P. R., Jenkins, J. T., & Butcher, J. T. (2012) · Biomechanics and Modeling in Mechanobiology · doi:10.1007/s10237-012-0424-5 · Cited by 31 · see citing works
How do avian embryos breathe? oxygen transport in the blood of early chick embryos
Cirotto, C., & Arangi, I. (1989) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(89)90602-6 · Cited by 31 · see citing works
Cardiac expression patterns of endothelin‐converting enzyme (ECE): Implications for conduction system development
Sedmera, D., Harris, B. S., Grant, E., et al. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21572 · Cited by 30 · see citing works
Patterns of muscular strain in the embryonic heart wall
Damon, B. J., Rémond, M. C., Bigelow, M. R., et al. (2009) · Developmental Dynamics · doi:10.1002/dvdy.21958 · Cited by 29 · see citing works
Effects of mechanical loading on early conduction system differentiation in the chick
Šaňková, B., Machálek, J., & Sedmera, D. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00721.2009 · Cited by 28 · see citing works
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
Chang, C. (1932) · The Anatomical Record · doi:10.1002/ar.1090510305 · Cited by 22 · see citing works
Morphologic study of the ascending aorta and aortic arch in hypoplastic left hearts: Surgical implications
Ilbawi, A., Spicer, D. E., Bharati, S., et al. (2007) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2007.01.070 · Cited by 19 · see citing works
Fibroblast Growth Factor-2 regulates proliferation of cardiac myocytes in normal and hypoplastic left ventricles in the developing chick
deAlmeida, A. C., & Sedmera, D. (2009) · Cardiology in the Young · doi:10.1017/s1047951109003552 · Cited by 18 · see citing works
Mathematical Modeling of Flow-Generated Forces in an In Vitro System of Cardiac Valve Development
Biechler, S. V., Potts, J. D., Yost, M. J., et al. (2009) · Annals of Biomedical Engineering · doi:10.1007/s10439-009-9824-9 · Cited by 17 · see citing works
Expression and Deposition of Fibrous Extracellular Matrix Proteins in Cardiac Valves during Chick Development
Tan, H., Junor, L., Price, R. L., Norris, R. A., Potts, J. D., & Goodwin, R. L. (2010) · Microscopy and Microanalysis · doi:10.1017/s1431927610094365 · Cited by 16 · see citing works
The Transitional Cardiac Pumping Mechanics in the Embryonic Heart
Johnson, B., Garrity, D. M., & Dasi, L. P. (2013) · Cardiovascular Engineering and Technology · doi:10.1007/s13239-013-0120-3 · Cited by 15 · see citing works
On the Role of Shear Stress in Cardiogenesis
Mironov, V. A., Visconti, R. P., & Markwald, R. R. (2005) · Endothelium · doi:10.1080/10623320500476708 · Cited by 13 · see citing works
The cycle of form and function in cardiac valvulogenesis
Lindsey, S. E., & Butcher, J. T. (2011) · Aswan Heart Centre Science & Practice Series · doi:10.5339/ahcsps.2011.10 · Cited by 13 · see citing works
Self-citation
Histochemical and Ultrastructural Changes in the Extracellular Matrix of the Developing Chick Semilunar Heart Valves
García‐Martínez, V., Sánchez‐Quintana, D., & Hurlé, J. M. (1991) · Cells Tissues Organs · doi:10.1159/000147166 · Cited by 12 · see citing works
[Principles of blood circulation of the heart].
Liebau, G. (1955) · PubMed · Cited by 10 · see citing works
A genetic blueprint for cardiac
Olson, E. N. (2000) · Cited by 4 · see citing works
Strain-Induced Tissue Growth Laws: Applications to Embryonic Cardiovascular Development
Rugonyi, S. (2013) · Journal of Applied Mechanical Engineering · doi:10.4172/2168-9873.s11-001 · Cited by 4 · see citing works
[Possibility of movement of blood in cardiovascular system without cardiac and venous valve function].
Liebau, G. (1956) · PubMed · Cited by 2 · see citing works

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Authors: Lindsey, S. E.
Venue: Frontiers in Physiology
Publisher: Frontiers Media SA
Published: 2014
Volume: 5
Pages: 318-318
ISSN: 1664-042X (ISSN-L)
DOI: 10.3389/fphys.2014.00318
PMC: PMC4140306
OpenAlex: W2017976972
Cited by: 159
References: 155
Citations by year: 2026: 7 · 2025: 12 · 2024: 17 · 2023: 13 · 2022: 17 · 2021: 16 · 2020: 14 · 2019: 16 · 2018: 14 · 2017: 10 · 2016: 15 · 2015: 7 · 2014: 1
FWCI: 1.04
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Physiology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Dogus University Institutional Repository (Dogus University) (submittedVersion, cc-by-nc-nd)
Funders: National Science Foundation
American Heart Association
Hartwell Foundation
European Commission (276987)
Fondation Leducq
Türkiye Bilimsel ve Teknolojik Araştırma Kurumu
National Heart, Lung, and Blood Institute (R01HL110328)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Keywords: heart development, mechanobiology, mechanical forces, hemodynamic flow, computational modeling, cardiac anomalies, cardiac signaling, congenital heart disease

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Mechanical regulation of cardiac development

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