The changing morphology of the ventricular walls of mouse and human with increasing gestation
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
PG/20/15/35041
British Heart Foundation - United Kingdom
PubMed
38284175
PubMed Central
PMC11095311
DOI
10.1111/joa.14017
Knihovny.cz E-zdroje
- Klíčová slova
- cardiac morphogenesis, compaction, excessive trabeculation, heart development, ventricular trabeculation,
- MeSH
- gestační stáří MeSH
- lidé MeSH
- myši MeSH
- srdeční komory * anatomie a histologie embryologie MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
That the highly trabeculated ventricular walls of the developing embryos transform to the arrangement during the fetal stages, when the mural architecture is dominated by the thickness of the compact myocardium, has been explained by the coalescence of trabeculations, often erroneously described as 'compaction'. Recent data, however, support differential rates of growth of the trabecular and compact layers as the major driver of change. Here, these processes were assessed quantitatively and visualized in standardized views. We used a larger dataset than has previously been available of mouse hearts, covering the period from embryonic day 10.5 to postnatal day 3, supported by images from human hearts. The volume of the trabecular layer increased throughout development, in contrast to what would be expected had there been 'compaction'. During the transition from embryonic to fetal life, the rapid growth of the compact layer diminished the proportion of trabeculations. Similarly, great expansion of the central cavity reduced the proportion of the total cavity made up of intertrabecular recesses. Illustrations of the hearts with the median value of left ventricular trabeculation confirm a pronounced growth of the compact wall, with prominence of the central cavity. This corresponds, in morphological terms, to a reduction in the extent of the trabecular layer. Similar observations were made in the human hearts. We conclude that it is a period of comparatively slow growth of the trabecular layer, rather than so-called compaction, that is the major determinant of the changing morphology of the ventricular walls of both mouse and human hearts.
Biosciences Institute Faculty of Medical Sciences Newcastle University Newcastle UK
Institute of Anatomy 1st Faculty of Medicine Charles University Prague Czech Republic
Institute of Dental Medicine 1st Faculty of Medicine Charles University Prague Czech Republic
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Anderson, R.H. & Bamforth, S.D. (2022) Morphogenesis of the mammalian aortic arch arteries. Frontiers in Cell and Development Biology, 10, 892900. PubMed PMC
Anderson, R.H. , Jensen, B. , Mohun, T.J. , Petersen, S.E. , Aung, N. , Zemrak, F. et al. (2017) Key questions relating to left ventricular noncompaction cardiomyopathy: is the emperor still wearing any clothes? The Canadian Journal of Cardiology, 33, 747–757. PubMed
Aung, N. , Doimo, S. , Ricci, F. , Sanghvi, M.M. , Pedrosa, C. , Woodbridge, S.P. et al. (2020) Prognostic significance of left ventricular noncompaction: systematic review and meta‐analysis of observational studies. Circulation Cardiovascular Imaging, 13, e009712. PubMed PMC
Axel, L. (2004) Papillary muscles do not attach directly to the solid heart wall. Circulation, 109, 3145–3148. PubMed
Blausen, B.E. , Johannes, R.S. & Hutchins, G.M. (1990) Computer‐based reconstructions of the cardiac ventricles of human embryos. American Journal of Cardiovascular Pathology, 3, 37–43. PubMed
Buffinton, C.M. , Faas, D. & Sedmera, D. (2013) Stress and strain adaptation in load‐dependent remodeling of the embryonic left ventricle. Biomechanics and Modeling in Mechanobiology, 12, 1037–1051. PubMed PMC
Chang, Y.H. , Sheftel, B.I. & Jensen, B. (2022) Anatomy of the heart with the highest heart rate. Journal of Anatomy, 241, 173–190. PubMed PMC
Chin, T.K. , Perloff, J.K. , Williams, R.G. , Jue, K. & Mohrmann, R. (1990) Isolated noncompaction of left ventricular myocardium. A Study of Eight Cases. Circulation, 82, 507–513. PubMed
de Bakker, B.S. , de Jong, K.H. , Hagoort, J. , de Bree, K. , Besselink, C.T. , de Kanter, F.E.C. et al. (2016) An interactive three‐dimensional digital atlas and quantitative database of human development. Science, 354, aag0053. PubMed
de Boer, B.A. , van den Berg, G. , de Boer, P.A. , Moorman, A.F. & Ruijter, J.M. (2012) Growth of the developing mouse heart: an interactive qualitative and quantitative 3D atlas. Developmental Biology, 368, 203–213. PubMed
de Lange, F.J. , Moorman, A.F. , Anderson, R.H. , Männer, J. , Soufan, A.T. , de Gier‐de Vries, C. et al. (2004) Lineage and morphogenetic analysis of the cardiac valves. Circulation Research, 95, 645–654. PubMed
Degenhardt, K. , Wright, A.C. , Horng, D. , Padmanabhan, A. & Epstein, J.A. (2010) Rapid 3D phenotyping of cardiovascular development in mouse embryos by micro‐CT with iodine staining. Circulation Cardiovascular Imaging, 3, 314–322. PubMed PMC
Faber, J.W. , Buijtendijk, M.F.J. , Klarenberg, H. , Vink, A.S. , Coolen, B.F. , Moorman, A.F.M. et al. (2022) Fetal tricuspid valve agenesis/atresia: testing predictions of the embryonic etiology. Pediatric Cardiology, 43, 796–806. PubMed
Faber, J.W. , D'Silva, A. , Christoffels, V.M. & Jensen, B. (2021) Lack of morphometric evidence for ventricular compaction in humans. Journal of Cardiology, 78, 397–405. PubMed
Faber, J.W. , Hagoort, J. , Moorman, A.F.M. , Christoffels, V.M. & Jensen, B. (2021) Quantified growth of the human embryonic heart. Biology Open, 10, bio057059. PubMed PMC
Faber, J.W. , Wüst, R.C.I. , Dierx, I. , Hummelink, J.A. , Kuster, D.W.D. , Nollet, E. et al. (2022) Equal force generation potential of trabecular and compact wall ventricular cardiomyocytes. iScience, 25, 105393. PubMed PMC
Finsterer, J. , Stollberger, C. & Towbin, J.A. (2017) Left ventricular noncompaction cardiomyopathy: cardiac, neuromuscular, and genetic factors. Nature Reviews Cardiology, 14, 224–237. PubMed
Gerger, D. , Stollberger, C. , Grassberger, M. , Gerecke, B. , Andresen, H. , Engberding, R. et al. (2013) Pathomorphologic findings in left ventricular hypertrabeculation/noncompaction of adults in relation to neuromuscular disorders. International Journal of Cardiology, 169, 249–253. PubMed
Geyer, S.H. , Mohun, T.J. & Weninger, W.J. (2009) Visualizing vertebrate embryos with episcopic 3D imaging techniques. ScientificWorldJournal, 9, 1423–1437. PubMed PMC
Gifford, C.A. , Ranade, S.S. , Samarakoon, R. , Salunga, H.T. , de Soysa, T.Y. , Huang, Y. et al. (2019) Oligogenic inheritance of a human heart disease involving a genetic modifier. Science, 364, 865–870. PubMed PMC
Gould, S.J. (1966) Allometry and size in ontogeny and phylogeny. Biological Reviews of the Cambridge Philosophical Society, 41, 587–640. PubMed
Gregorovicova, M. , Bartos, M. , Jensen, B. , Janacek, J. , Minne, B. , Moravec, J. et al. (2022) Anguimorpha as a model group for studying the comparative heart morphology among Lepidosauria: evolutionary window on the ventricular septation. Ecology and Evolution, 12, e9476. PubMed PMC
Grothoff, M. , Pachowsky, M. , Hoffmann, J. , Posch, M. , Klaassen, S. , Lehmkuhl, L. et al. (2012) Value of cardiovascular MR in diagnosing left ventricular non‐compaction cardiomyopathy and in discriminating between other cardiomyopathies. European Radiology, 22, 2699–2709. PubMed PMC
Gundersen, H.J. , Bendtsen, T.F. , Korbo, L. , Marcussen, N. , Møller, A. , Nielsen, K. et al. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS, 96, 379–394. PubMed
Hanemaaijer, J. , Gregorovicova, M. , Nielsen, J.M. , Moorman, A.F.M. , Wang, T. , Planken, R.N. et al. (2019) Identification of the building blocks of ventricular septation in monitor lizards (Varanidae). Development, 146, dev177121. PubMed
Henderson, D.J. & Anderson, R.H. (2009) The development and structure of the ventricles in the human heart. Pediatric Cardiology, 30, 588–596. PubMed
Hussein, A. , Karimianpour, A. , Collier, P. & Krasuski, R.A. (2015) Isolated noncompaction of the left ventricle in adults. Journal of the American College of Cardiology, 66, 578–585. PubMed
Ishiwata, T. , Nakazawa, M. , Pu, W.T. , Tevosian, S.G. & Izumo, S. (2003) Developmental changes in ventricular diastolic function correlate with changes in ventricular myoarchitecture in normal mouse embryos. Circulation Research, 93, 857–865. PubMed
Jensen, B. , Agger, P. , de Boer, B.A. , Oostra, R.J. , Pedersen, M. , van der Wal, A.C. et al. (2016) The hypertrabeculated (noncompacted) left ventricle is different from the ventricle of embryos and ectothermic vertebrates. Biochimica et Biophysica Acta, 1863, 1696–1706. PubMed
Jensen, B. & Petersen, S.E. (2022) Making less of a mess of the trabecular mesh. Radiology: Cardiothoracic Imaging, 4, e220227. PubMed PMC
Jensen, B. , Salvatori, D. , Schouten, J. , Meijborg, V.M.F. , Lauridsen, H. & Agger, P. (2024) Trabeculations of the Porcine and Human Cardiac Ventricles Are Different in Number but Similar in Total Volume. Clinical Anatomy. 10.1002/ca.24135 PubMed DOI
Jensen, B. & Smith, T.H. (2018) Examples of weak, if not absent, Form‐Function Relations in the Vertebrate Heart. Journal of Cardiovascular Devlopment and Disease, 5, 46. PubMed PMC
Jensen, B. , Wang, T. , Christoffels, V.M. & Moorman, A.F. (2013) Evolution and development of the building plan of the vertebrate heart. Biochimica et Biophysica Acta, 1833, 783–794. PubMed
Luu, J.M. , Gebhard, C. , Ramasundarahettige, C. , Desai, D. , Schulze, K. , Marcotte, F. et al. (2022) Normal sex and age‐specific parameters in a multi‐ethnic population: a cardiovascular magnetic resonance study of the Canadian Alliance for healthy hearts and minds cohort. Journal of Cardiovascular Magnetic Resonance, 24, 2. PubMed PMC
Manner, J. (2022) When does the human embryonic heart start beating? A review of contemporary and historical sources of knowledge about the onset of blood circulation in man. Journal of Cardiovascular Devlopment and Disease, 9(6), 187. PubMed PMC
Moorman, A.F. & Christoffels, V.M. (2003) Cardiac chamber formation: development, genes, and evolution. Physiological Reviews, 83, 1223–1267. PubMed
Oechslin, E. & Jenni, R. (2011) Left ventricular non‐compaction revisited: a distinct phenotype with genetic heterogeneity? European Heart Journal, 32, 1446–1456. PubMed
Olejnickova, V. , Kocka, M. , Kvasilova, A. , Kolesova, H. , Dziacky, A. , Gidor, T. et al. (2021) Gap junctional communication via Connexin43 between Purkinje fibers and working myocytes explains the Epicardial activation pattern in the postnatal mouse left ventricle. International Journal of Molecular Sciences, 22(5), 2475. PubMed PMC
Petersen, S.E. , Jensen, B. , Aung, N. , Friedrich, M.G. , McMahon, C. , Mohiddin, S.A. et al. (2023) Excessive Trabeculation of the left ventricle: JACC: cardiovascular imaging expert panel paper. JACC: Cardiovascular Imaging, 16, 408–425. PubMed PMC
Polacin, M. , Karolyi, M. , Wilzeck, V. , Eberhard, M. , Gotschy, A. , Alkadhi, H. et al. (2022) Three‐dimensional whole‐heart cardiac MRI sequence for measuring Trabeculation in left ventricular noncompaction. Radiology: Cardiothoracic Imaging, 4, e220109. PubMed PMC
Riekerk, H.C.E. , Coolen, B.F. , Strijkers, G.J. et al. (2022) Higher spatial resolution improves the interpretation of the extent of ventricular trabeculation. Journal of Anatomy, 240, 357–375. PubMed PMC
Ross, S.B. , Jones, K. , Blanch, B. , Puranik, R. , McGeechan, K. , Barratt, A. et al. (2020) A systematic review and meta‐analysis of the prevalence of left ventricular non‐compaction in adults. European Heart Journal, 41, 1428–1436. PubMed
Rowlatt, U. (1990) Comparative anatomy of the heart of mammals. Zoological Journal of the Linnean Society, 98, 73–110.
Rychterova, V. (1971) Principle of growth in thickness of the heart ventricular wall in the chick embryo. Folia Morphol (Praha), 19, 262–272. PubMed
Sankova, B. , Benes, J., Jr. , Krejci, E. , Dupays, L. , Theveniau‐Ruissy, M. , Miquerol, L. et al. (2012) The effect of connexin40 deficiency on ventricular conduction system function during development. Cardiovascular Research, 95, 469–479. PubMed
Sedmera, D. , Grobety, M. , Reymond, C. , Baehler, P. , Kucera, P. & Kappenberger, L. (1999) Pacing‐induced ventricular remodeling in the chick embryonic heart. Pediatric Research, 45, 845–852. PubMed
Sedmera, D. , Reckova, M. , DeAlmeida, A. , Coppen, S.R. , Kubalak, S.W. , Gourdie, R.G. et al. (2003) Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anatomical Record Part A, Discoveries in Molecular, Cellular, and Evoloutionary Biology, 274, 773–777. PubMed
Shi, W. , Scialdone, A.P. , Emerson, J.I. , Mei, L. , Wasson, L.K. , Davies, H.A. et al. (2023) Missense mutation in human CHD4 causes ventricular noncompaction by repressing ADAMTS1. Circulation Research, 133, 48–67. PubMed PMC
Smerup, M. , Nielsen, E. , Agger, P. , Frandsen, J. , Vestergaard‐Poulsen, P. , Andersen, J. et al. (2009) The three‐dimensional arrangement of the myocytes aggregated together within the mammalian ventricular myocardium. Anatomical Record (Hoboken), 292, 1–11. PubMed
Tang, J. , Zhu, H. , Tian, X. , Wang, H. , Liu, S. , Liu, K. et al. (2022) Extension of endocardium‐derived vessels generate coronary arteries in neonates. Circulation Research, 130, 352–365. PubMed
Tian, X. , Li, Y. , He, L. , Zhang, H. , Huang, X. , Liu, Q. et al. (2017) Identification of a hybrid myocardial zone in the mammalian heart after birth. Nature Communications, 8, 87. PubMed PMC
Tyser, R.C.V. & Srinivas, S. (2020) The first heartbeat‐origin of cardiac contractile activity. Cold Spring Harbor Perspectives in Biology, 12(7), a037135. PubMed PMC
van der Ven, J.P.G. , Sadighy, Z. , Valsangiacomo Buechel, E.R. , Sarikouch, S. , Robbers‐Visser, D. , Kellenberger, C.J. et al. (2020) Multicentre reference values for cardiac magnetic resonance imaging derived ventricular size and function for children aged 0‐18 years. European Heart Journal Cardiovascular Imaging, 21, 102–113. PubMed PMC
Van Mierop, L.H. & Bertuch, C.J., Jr. (1967) Development of arterial blood pressure in the chick embryo. Am . The Journal of Physiology, 212, 43–48. PubMed
van Weerd, J.H. & Christoffels, V.M. (2016) The formation and function of the cardiac conduction system. Development, 143, 197–210. PubMed
Wang, J. , Liu, S. , Heallen, T. & Martin, J.F. (2018) The hippo pathway in the heart: pivotal roles in development, disease, and regeneration. Nature Reviews Cardiology, 15, 672–684. PubMed
Wilsbacher, L. & McNally, E.M. (2016) Genetics of cardiac developmental disorders: Cardiomyocyte proliferation and growth and relevance to heart failure. Annual Review of Pathology, 11, 395–419. PubMed PMC