Development of ventricular trabeculae affects electrical conduction in the early endothermic heart
Language English Country United States Media print-electronic
Document type Journal Article
Grant support
NU21J-02-00039
Czech Health Research Council
22-05271S
Czech Science Foundation
National Institute for Research of Metabolic and Cardiovascular Diseases (Programme EXCELES, ID Project No. LX22NPO5104) - Funded by the European Union - Next Generation EU.
PubMed
36400745
DOI
10.1002/dvdy.552
Knihovny.cz E-resources
- Keywords
- Nkx2.5, embryonic chick heart, neuregulin/ErbB, ventricular trabeculae,
- MeSH
- Neuregulins MeSH
- Mammals MeSH
- Heart * MeSH
- Heart Ventricles * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Neuregulins MeSH
BACKGROUND: The ventricular trabeculae play a role, among others, in the impulse spreading in ectothermic hearts. Despite the morphological similarity with the early developing hearts of endotherms, this trabecular function in mammalian and avian embryos was poorly addressed. RESULTS: We simulated impulse propagation inside the looping ventricle and revealed delayed apical activation in the heart with inhibited trabecular growth. This finding was corroborated by direct imaging of the endocardial surface showing early activation within the trabeculae implying preferential spreading of depolarization along with them. Targeting two crucial pathways of trabecular formation (Neuregulin/ErbB and Nkx2.5), we showed that trabecular development is also essential for proper conduction patterning. Persistence of the slow isotropic conduction likely contributed to the pumping failure in the trabeculae-deficient hearts. CONCLUSIONS: Our results showed the essential role of trabeculae in intraventricular impulse spreading and conduction patterning in the early endothermic heart. Lack of trabeculae leads to the failure of conduction parameters differentiation resulting in primitive ventricular activation with consequent impact on the cardiac pumping function.
Institute of Anatomy 1st Faculty of Medicine Charles University Prague Czech Republic
Laboratory of Biomathematics Institute of Physiology Czech Academy of Sciences Prague Czech Republic
See more in PubMed
Moorman AFM, Christoffels VM. Development of the cardiac conduction system: a matter of chamber development. Novartis Found Symp. 2003;250:25-34. discussion 34-43, 276-279.
Kamino K, Hirota A, Fujii S. Localization of pacemaking activity in early embryonic heart monitored using voltage-sensitive dye. Nature. 1981;290(5807):595-597. doi:10.1038/290595a0
Hirota A, Kamino K, Komuro H, Sakai T, Yada T. Early events in development of electrical activity and contraction in embryonic rat heart assessed by optical recording. J Physiol. 1985;369:209-227. doi:10.1113/jphysiol.1985.sp015897
Christoffels VM, Burch JBE, Moorman AFM. Architectural plan for the heart: early patterning and delineation of the chambers and the nodes. Trends Cardiovasc Med. 2004;14(8):301-307. doi:10.1016/j.tcm.2004.09.002
Chuck ET, Freeman DM, Watanabe M, Rosenbaum DS. Changing activation sequence in the embryonic chick heart. Implications for the development of the his-Purkinje system. Circ Res. 1997;81(4):470-476. doi:10.1161/01.res.81.4.470
Chuck ET, Meyers K, France D, Creazzo TL, Morley GE. Transitions in ventricular activation revealed by two-dimensional optical mapping. Anat Rec. 2004;280A(2):990-1000. doi:10.1002/ar.a.20083
de Jong F, Opthof T, Wilde AA, et al. Persisting zones of slow impulse conduction in developing chicken hearts. Circ Res. 1992;71(2):240-250.
Rentschler S, Vaidya DM, Tamaddon H, et al. Visualization and functional characterization of the developing murine cardiac conduction system. Development. 2001;128(10):1785-1792.
Sankova B, Benes J, Krejci E, et al. The effect of connexin40 deficiency on ventricular conduction system function during development. Cardiovasc Res. 2012;95(4):469-479. doi:10.1093/cvr/cvs210
Sedmera D, Reckova M, Bigelow MR, et al. Developmental transitions in electrical activation patterns in chick embryonic heart. Anat Rec. 2004;280A(2):1001-1009. doi:10.1002/ar.a.20107
Challice CE, Virágh S. The phylogenetic and ontogenetic development of the mammalian heart: some theoretical considerations. Acta Biochim Biophys Acad Sci Hung. 1974;9(1-2):131-140.
Arbel ER, Liberthson R, Langendorf R, Pick A, Lev M, Fishman AP. Electrophysiological and anatomical observations on the heart of the African lungfish. Am J Physiol. 1977;232(1):H24-H34. doi:10.1152/ajpheart.1977.232.1.H24
Sedmera D, Reckova M, de Almeida A, et al. Functional and morphological evidence for a ventricular conduction system in zebrafish and Xenopus hearts. Am J Physiol Heart Circ Physiol. 2003;284(4):H1152-H1160. doi:10.1152/ajpheart.00070.2002
Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn. 1992;195(4):231-272. doi:10.1002/aja.1001950404
Lantuejoul C, Beucher S. On the use of the geodesic metric in image analysis. J Microsc. 1981;121(1):39-49. doi:10.1111/j.1365-2818.1981.tb01197.x
Olejnickova V, Sankova B, Sedmera D, Janacek J. Trabecular architecture determines impulse propagation through the early embryonic mouse heart. Front Physiol. 2018;9:1876. doi:10.3389/fphys.2018.01876
Icardo JM, Fernandez-Terán A. Morphologic study of ventricular trabeculation in the embryonic chick heart. Acta Anat (Basel). 1987;130(3):264-274. doi:10.1159/000146455
Sedmera D, Pexieder T, Hu N, Clark EB. Developmental changes in the myocardial architecture of the chick. Anat Rec. 1997;248(3):421-432. doi:10.1002/(SICI)1097-0185(199707)248:3<421::AID-AR15>3.0.CO;2-R
Liu J, Bressan M, Hassel D, et al. A dual role for ErbB2 signaling in cardiac trabeculation. Development. 2010;137(22):3867-3875. doi:10.1242/dev.053736
Peshkovsky C, Totong R, Yelon D. Dependence of cardiac trabeculation on neuregulin signaling and blood flow in zebrafish. Dev Dyn. 2011;240(2):446-456. doi:10.1002/dvdy.22526
Rasouli SJ, Stainier DYR. Regulation of cardiomyocyte behavior in zebrafish trabeculation by Neuregulin 2a signaling. Nat Commun. 2017;8(1):15281. doi:10.1038/ncomms15281
Donna L, Xifu L, Ariel F, et al. Neuregulin 1 sustains the gene regulatory network in both trabecular and nontrabecular myocardium. Circ Res. 2010;107(6):715-727. doi:10.1161/CIRCRESAHA.110.218693
Britsch S, Li L, Kirchhoff S, et al. The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 1998;12(12):1825-1836. doi:10.1101/gad.12.12.1825
Miquerol L, Meysen S, Mangoni M, et al. Architectural and functional asymmetry of the his-Purkinje system of the murine heart. Cardiovasc Res. 2004;63(1):77-86. doi:10.1016/j.cardiores.2004.03.007
Sedmera D, Reckova M, DeAlmeida A, et al. Spatiotemporal pattern of commitment to slowed proliferation in the embryonic mouse heart indicates progressive differentiation of the cardiac conduction system. Anatl Rec. 2003;274A(1):773-777. doi:10.1002/ar.a.10085
Jensen B, van der Wal AC, Moorman AFM, Christoffels VM. Excessive trabeculations in noncompaction do not have the embryonic identity. Int J Cardiol. 2017;227:325-330. doi:10.1016/j.ijcard.2016.11.089
Jensen B, Agger P, de Boer BA, et al. The hypertrabeculated (noncompacted) left ventricle is different from the ventricle of embryos and ectothermic vertebrates. Biochim Biophys Acta. 2016;1863((7, Part B)):1696-1706. doi:10.1016/j.bbamcr.2015.10.018
Joyce W, Wang T. What determines systemic blood flow in vertebrates? J Exp Biol. 2020;223(4):1-15. doi:10.1242/jeb.215335
Reckova M, Rosengarten C, de Almeida A, et al. Hemodynamics is a key epigenetic factor in development of the cardiac conduction system. Circ Res. 2003;93(1):77-85. doi:10.1161/01.RES.0000079488.91342.B7
Clark EB, Hu N, Dummett JL, Vandekieft GK, Olson C, Tomanek R. Ventricular function and morphology in chick embryo from stages 18 to 29. Am J Physiol. 1986;250(3 Pt 2):H407-H413. doi:10.1152/ajpheart.1986.250.3.H407
Girard H. Arterial pressure in the chick embryo. Am J Physiol. 1973;224(2):454-460. doi:10.1152/ajplegacy.1973.224.2.454
Struijk PC, Mathews VJ, Loupas T, et al. Blood pressure estimation in the human fetal descending aorta. Ultrasound Obstet Gynecol. 2008;32(5):673-681. doi:10.1002/uog.6137
Del Monte-Nieto G, Ramialison M, Adam AAS, et al. Control of cardiac jelly dynamics by NOTCH1 and NRG1 defines the building plan for trabeculation. Nature. 2018;557(7705):439-445. doi:10.1038/s41586-018-0110-6
Staudt DW, Liu J, Thorn KS, Stuurman N, Liebling M, Stainier DYR. High-resolution imaging of cardiomyocyte behavior reveals two distinct steps in ventricular trabeculation. Development. 2014;141(3):585-593. doi:10.1242/dev.098632
Abramochkin DV, Rozenshtraukh LV. Optical mapping of chronotopography of excitation of the frog heart ventricle epicardial surface in sinus rhythm. Ross Fiziol Zh Im I M Sechenova. 2008;94(4):414-420.
Jensen B, Boukens BJ, Crossley DA II, et al. Specialized impulse conduction pathway in the alligator heart. eLife. 2018;7:e32120. doi:10.7554/eLife.32120
Kvasilova A, Olejnickova V, Jensen B, et al. The formation of the atrioventricular conduction axis is linked in development to ventricular septation. J Exp Biol. 2020;223(Pt 19):1-5. doi:10.1242/jeb.229278
Jensen B, Boukens BJD, Postma AV, et al. Identifying the evolutionary building blocks of the cardiac conduction system. PLoS One. 2012;7(9):e44231. doi:10.1371/journal.pone.0044231
Vaykshnorayte MA, Azarov JE, Tsvetkova AS, Vityazev VA, Ovechkin AO, Shmakov DN. The contribution of ventricular apicobasal and transmural repolarization patterns to the development of the T wave body surface potentials in frogs (Rana temporaria) and pike (Esox lucius). Comp Biochem Physiol A Mol Integr Physiol. 2011;159(1):39-45. doi:10.1016/j.cbpa.2011.01.016
Vityazev VA, Azarov JE. Stretch-excitation correlation in the toad heart. J Exp Biol. 2020;223(Pt 23):1-5. doi:10.1242/jeb.228882
Jensen B, Moorman AFM, Wang T. Structure and function of the hearts of lizards and snakes. Biol Rev Camb Philos Soc. 2014;89(2):302-336. doi:10.1111/brv.12056
Stephenson A, Adams JW, Vaccarezza M. The vertebrate heart: an evolutionary perspective. J Anat. 2017;231(6):787-797. doi:10.1111/joa.12687
Virágh S, Challice CE. The development of the conduction system in the mouse embryo heart. I. the first embryonic A-V conduction pathway. Dev Biol. 1977;56(2):382-396.
Rentschler S, Zander J, Meyers K, et al. Neuregulin-1 promotes formation of the murine cardiac conduction system. Proc Natl Acad Sci U S A. 2002;99(16):10464-10469. doi:10.1073/pnas.162301699
Samsa LA, Yang B, Liu J. Embryonic cardiac chamber maturation: Trabeculation, conduction and Cardiomyocyte proliferation. Am J Med Genet C Semin Med Genet. 2013;163(3):157-168. doi:10.1002/ajmg.c.31366
Budi EH, Patterson LB, Parichy DM. Embryonic requirements for ErbB signaling in neural crest development and adult pigment pattern formation. Development. 2008;135(15):2603-2614. doi:10.1242/dev.019299
Lyons DA, Pogoda HM, Voas MG, et al. erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr Biol. 2005;15(6):513-524. doi:10.1016/j.cub.2005.02.030
Scherz PJ, Huisken J, Sahai-Hernandez P, Stainier DYR. High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development. 2008;135(6):1179-1187. doi:10.1242/dev.010694
Dupays L, Jarry-Guichard T, Mazurais D, et al. Dysregulation of connexins and inactivation of NFATc1 in the cardiovascular system of Nkx2-5 null mutants. J Mol Cell Cardiol. 2005;38(5):787-798. doi:10.1016/j.yjmcc.2005.02.021
Christoffels VM, Mommersteeg MTM, Trowe MO, et al. Formation of the venous pole of the heart from an Nkx2-5-negative precursor population requires Tbx18. Circ Res. 2006;98(12):1555-1563. doi:10.1161/01.RES.0000227571.84189.65
Ye W, Wang J, Song Y, et al. A common Shox2-Nkx2-5 antagonistic mechanism primes the pacemaker cell fate in the pulmonary vein myocardium and sinoatrial node. Development. 2015;142(14):2521-2532. doi:10.1242/dev.120220
Espinoza-Lewis RA, Liu H, Sun C, Chen C, Jiao K, Chen Y. Ectopic expression of Nkx2.5 suppresses the formation of the sinoatrial node in mice. Dev Biol. 2011;356(2):359-369. doi:10.1016/j.ydbio.2011.05.663
Liang X, Wang G, Lin L, et al. HCN4 dynamically marks the first heart field and conduction system precursors. Circ Res. 2013;113(4):399-407. doi:10.1161/CIRCRESAHA.113.301588
Wiese C, Grieskamp T, Airik R, et al. Formation of the sinus node head and differentiation of sinus node myocardium are independently regulated by Tbx18 and Tbx3. Circ Res. 2009;104(3):388-397. doi:10.1161/CIRCRESAHA.108.187062
Li H, Li D, Wang Y, et al. Nkx2-5 defines a subpopulation of pacemaker cells and is essential for the physiological function of the sinoatrial node in mice. Development. 2019;146((14)):dev178145. doi:10.1242/dev.178145
Keller BB, MacLennan MJ, Tinney JP, Yoshigi M. In vivo assessment of embryonic cardiovascular dimensions and function in day-10.5 to −14.5 mouse embryos. Circ Res. 1996;79(2):247-255. doi:10.1161/01.res.79.2.247
Phoon CKL, Ji RP, Aristizábal O, et al. Embryonic heart failure in NFATc1−/− mice: novel mechanistic insights from in utero ultrasound biomicroscopy. Circ Res. 2004;95(1):92-99. doi:10.1161/01.RES.0000133681.99617.28
Kockova R, Svatunkova J, Novotny J, Hejnova L, Ostadal B, Sedmera D. Heart rate changes mediate the embryotoxic effect of antiarrhythmic drugs in the chick embryo. Am J Physiol Heart Circ Physiol. 2013;304(6):H895-H902. doi:10.1152/ajpheart.00679.2012
Kasahara H, Ueyama T, Wakimoto H, et al. Nkx2.5 homeoprotein regulates expression of gap junction protein connexin 43 and sarcomere organization in postnatal cardiomyocytes. J Mol Cell Cardiol. 2003;35(3):243-256. doi:10.1016/s0022-2828(03)00002-6
Kasahara H, Wakimoto H, Liu M, et al. Progressive atrioventricular conduction defects and heart failure in mice expressing a mutant Csx/Nkx2.5 homeoprotein. J Clin Invest. 2001;108(2):189-201. doi:10.1172/JCI12694
Linhares VLF, Almeida NAS, Menezes DC, et al. Transcriptional regulation of the murine Connexin40 promoter by cardiac factors Nkx2-5, GATA4 and Tbx5. Cardiovasc Res. 2004;64(3):402-411. doi:10.1016/j.cardiores.2004.09.021
Biben C, Weber R, Kesteven S, et al. Cardiac septal and valvular dysmorphogenesis in mice heterozygous for mutations in the homeobox gene Nkx2-5. Circ Res. 2000;87(10):888-895.
Martinsen BJ. Reference guide to the stages of chick heart embryology. Dev Dyn. 2005;233(4):1217-1237. doi:10.1002/dvdy.20468
Metscher BD. MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn. 2009;238(3):632-640. doi:10.1002/dvdy.21857
Olejnickova V, Sedmera D. What is the optimal light source for optical mapping using voltage- and calcium-sensitive dyes? Physiol Res. 2020;69(4):599-607. doi:10.33549/physiolres.934471
Kolarova J, Novakova M, Ronzhina M, et al. Isolated rabbit hearts-Databases of EGs and MAP signals. Computing in Cardiology Conference, Zaragoza, Spain, 2013. IEEE; 2013:551-554. Accessed July 7, 2017 http://ieeexplore.ieee.org/abstract/document/6713436/
Vostarek F, Svatunkova J, Sedmera D. Acute temperature effects on function of the chick embryonic heart. Acta Physiol. 2016;217(4):276-286. doi:10.1111/apha.12691
Kolesova H, Capek M, Radochova B, Janacek J, Sedmera D. Comparison of different tissue clearing methods and 3D imaging techniques for visualization of GFP-expressing mouse embryos and embryonic hearts. Histochem Cell Biol. 2016;146(2):141-152.
Miller CE, Thompson RP, Bigelow MR, Gittinger G, Trusk TC, Sedmera D. Confocal imaging of the embryonic heart: how deep? Microsc Microanal. 2005;11(3):216-223. doi:10.1017/S1431927605050464