Ventricular anisotropic deformation and contractile function of the developing heart of zebrafish in vivo.

cardiac development ventricle ventricular deformation ventricular function ventricular trabeculae zebrafish embryos

Journal

Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927

Informations de publication

Date de publication:
02 2023
Historique:
revised: 10 08 2022
received: 18 02 2022
accepted: 29 08 2022
pubmed: 5 9 2022
medline: 15 2 2023
entrez: 4 9 2022
Statut: ppublish

Résumé

The developing zebrafish ventricle generates higher intraventricular pressure (IVP) with increasing stroke volume and cardiac output at different developmental stages to meet the metabolic demands of the rapidly growing embryo (Salehin et al. Ann Biomed Eng, 2021;49(9): 2080-2093). To understand the changing role of the developing embryonic heart, we studied its biomechanical characteristics during in vivo cardiac cycles. By combining changes in wall strains and IVP measurements, we assessed ventricular wall stiffness during diastolic filling and the ensuing systolic IVP-generation capacity during 3-, 4-, and 5-day post fertilization (dpf). We further examined the anisotropy of wall deformation, in different regions within the ventricle, throughout a complete cardiac cycle. We found the ventricular walls grow increasingly stiff during diastolic filling with a corresponding increase in IVP-generation capacity from 3- to 4- and 5-dpf groups. In addition, we found the corresponding increasing level of anisotropic wall deformation through cardiac cycles that favor the latitudinal direction, with the most pronounced found in the equatorial region of the ventricle. From 3- to 4- and 5-dpf groups, the ventricular wall myocardium undergoes increasing level of anisotropic deformation. This, in combination with the increasing wall stiffness and IVP-generation capacity, allows the developing heart to effectively pump blood to meet the rapidly growing embryo's needs.

Sections du résumé

BACKGROUND
The developing zebrafish ventricle generates higher intraventricular pressure (IVP) with increasing stroke volume and cardiac output at different developmental stages to meet the metabolic demands of the rapidly growing embryo (Salehin et al. Ann Biomed Eng, 2021;49(9): 2080-2093). To understand the changing role of the developing embryonic heart, we studied its biomechanical characteristics during in vivo cardiac cycles. By combining changes in wall strains and IVP measurements, we assessed ventricular wall stiffness during diastolic filling and the ensuing systolic IVP-generation capacity during 3-, 4-, and 5-day post fertilization (dpf). We further examined the anisotropy of wall deformation, in different regions within the ventricle, throughout a complete cardiac cycle.
RESULTS
We found the ventricular walls grow increasingly stiff during diastolic filling with a corresponding increase in IVP-generation capacity from 3- to 4- and 5-dpf groups. In addition, we found the corresponding increasing level of anisotropic wall deformation through cardiac cycles that favor the latitudinal direction, with the most pronounced found in the equatorial region of the ventricle.
CONCLUSIONS
From 3- to 4- and 5-dpf groups, the ventricular wall myocardium undergoes increasing level of anisotropic deformation. This, in combination with the increasing wall stiffness and IVP-generation capacity, allows the developing heart to effectively pump blood to meet the rapidly growing embryo's needs.

Identifiants

pubmed: 36057940
doi: 10.1002/dvdy.536
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

247-262

Subventions

Organisme : National Science Foundation
ID : 1936519

Informations de copyright

© 2022 American Association for Anatomy.

Références

Salehin N, Villarreal C, Teranikar T, Dubansky B, Lee J, Chuong C-J. Assessing pressure-volume relationship in developing heart of zebrafish in-vivo. Ann Biomed Eng. 2021;49:2080-2093. doi:10.1007/s10439-021-02731-0
Bartman T, Hove J. Mechanics and function in heart morphogenesis. Dev Dyn. 2005;233:373-381.
Taber LA, Perucchio R. Modeling heart development. J Elasticity. 2000;61:165-197.
Brown DR, Samsa LA, Qian L, Liu J. Advances in the study of heart development and disease using zebrafish. J Cardiovasc Dev Dis. 2016;3(2):13. doi:10.3390/jcdd3020013
Lee J, Fei P, Sevag Packard RR, et al. 4-dimensional light-sheet microscopy to elucidate shear stress modulation of cardiac trabeculation. J Clin Investig. 2016;126(5):1679-1690. doi:10.1172/jci83496
Scherz PJ, Huisken J, Sahai-Hernandez P, Stainier DY. High-speed imaging of developing heart valves reveals interplay of morphogenesis and function. Development. 2008;135:1179-1187.
Vermot J, Forouhar AS, Liebling M, et al. Reversing blood flows act through klf2a to ensure normal valvulogenesis in the developing heart. PLoS Biol. 2009;7(11):e1000246. doi:10.1371/journal.pbio.1000246
Yalcin HC, Amindari A, Butcher JT, Althani A, Yacoub M. Heart function and hemodynamic analysis for zebrafish embryos. Dev Dyn. 2017;246:868-880.
Voronov DA, Alford PW, Xu G, Taber LA. The role of mechanical forces in dextral rotation during cardiac looping in the chick embryo. Dev Biol. 2004;272:339-350.
Stekelenburg-de Vos S, Steendijk P, Ursem NT, Wladimiroff JW, Poelmann RE. Systolic and diastolic ventricular function in the normal and extra-embryonic venous clipped chicken embryo of stage 24: a pressure-volume loop assessment. Ultrasound Obstet Gynecol. 2007;30:325-331.
Tobita K, Schroder EA, Tinney JP, Garrison JB, Keller BB. Regional passive ventricular stress-strain relations during development of altered loads in chick embryo. Am J Physiol Heart Circ Physiol. 2002;282:H2386-H2396.
Teranikar, T., Villarreal, C., Salehin, N., Ijaseun, T., Lim, J., Dominguez, C., Nguyen, V., Cao, H., Chuong, C. J., & Lee, J. Scale space detector for analyzing spatiotemporal ventricular contractility and nuclear morphogenesis in zebrafish. iScience, 2022; 25(9), 104876. 10.1016/j.isci.2022.104876
Fung YC. Biomechanics: motion, flow, stress, and growth. Berlin, Germany: Springer-Verlag; 1990.
Taber LA, Hu N, Pexieder T, Clark EB, Keller BB. Residual strain in the ventricle of the stage 16-24 Chick embryo. Circulation Res. 1993;72:455-462.
Fung YC. A First Course in Continuum Mechanics. 3rd ed. Pearson; 1993.
Ishiwata T, Nakazawa M, Pu WT, Tevosian SG, Izumo S. Developmental changes in ventricular diastolic function correlate with changes in ventricular myoarchitecture in normal mouse embryos. Circ Res. 2003;93:857-865.
Bagatto B, Burggren W. A three-dimensional functional assessment of heart and vessel development in the larva of the zebrafish (Danio rerio). Physiol Biochem Zool. 2005;79:194-201.
Waldman LK, Fung YC, Covell JW. Transmural myocardial deformation in the canine left ventricle. Normal in vivo three-dimensional finite strains. Circ Res. 1985;57:152-163.
Chuong CJ, Sacks MS, Templeton G, Schwiep F, Johnson RL Jr. Regional deformation and contractile function in canine right ventricular free wall. AJP - Heart and Circulatory Physiology. 1991;260:H1224-H1235.
Tobita K, Keller BB. Right and left ventricular wall deformation patterns in normal and left heart hypoplasia chick embryos. Am J Physiol Heart Circ Physiol. 2000;279:H959-H969.
Waldman LK, Nosan D, Villarreal F, Covell JW. Relation between transmural deformation and local myofiber direction in canine left ventricle. Circ Res. 1988;63:550-562.
Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn. 1992;195:231-272.
Tobita K, Garrison JB, Liu LJ, Tinney JP, Keller BB. Three-dimensional myofiber architecture of the embryonic left ventricle during normal development and altered mechanical loads. Anat Rec A Discov Mol Cell Evol Biol. 2005;283:193-201.
Gendernalik A, Zebhi B, Ahuja N, Garrity D, Bark D. In vivo pressurization of the zebrafish embryonic heart as a tool to characterize tissue properties during development. Ann Biomed Eng. 2021;49:834-845.
Majkut S, Idema T, Swift J, Krieger C, Liu A, Discher DE. Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr Biol. 2013;23:2434-2439.
Rasouli SJ, Stainier DYR. Regulation of cardiomyocyte behavior in zebrafish trabeculation by neuregulin 2a signaling. Nat Commun. 2017;8:15281.
Uribe V, Ramadass R, Dogra D, et al. Stainier, in vivo analysis of cardiomyocyte proliferation during trabeculation. Development. 2018;145:dev164194. doi:10.1242/dev.164194
Hu N, Sedmera D, Yost HJ, Clark EB. Structure and function of the developing zebrafish heart. Anat Rec. 2000;260:148-157. doi:10.1002/1097-0185(20001001)260:2<148::AID-AR50>3.0.CO;2-X
Hu N, Yost HJ, Clark EB. Cardiac morphology and blood pressure in the adult zebrafish. Anat Rec. 2001;264(1):1-12. doi:10.1002/ar.1111 PMID: 11505366.
Buffinton CM, Faas D, Sedmera D. Stress and strain adaptation in load-dependent remodeling of the embryonic left ventricle. Biomech Model Mechanobiol. 2013;12(5):1037-1051. doi:10.1007/s10237-012-0461-0
Sonnenblick EH, Ross J, Covell JW, Spotnitz HM, Spiro D. The ultrastructure of the heart in systole and diastole: >changes in sarcomere length. Circ Res. 1967;21:423-431.
Ebert AM, Hume GL, Warren KS, et al. Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts. Proc Natl Acad Sci U S A. 2005;102:17705-17710.
Radke MH, Peng J, Wu Y, et al. Targeted deletion of titin n2b region leads to diastolic dysfunction and cardiac atrophy. Proc Natl Acad Sci U S A. 2007;104:3444-3449.
Huisken J, Stainier DYR. Selective plane illumination microscopy techniques in developmental biology. Development (Cambridge). 2009;136:1963-1975.
Mably JD, Mohideen MA, Burns CG, Chen JN, Fishman MC. Heart of glass regulates the concentric growth of the heart in Zebrafish. Curr Biol. 2003;13(24):2138-2147. doi:10.1016/j.cub.2003.11.055
Peshkovsky C, Totong R, Yelon D. Dependence of cardiac trabeculation on neuregulin signaling and blood flow in zebrafish. Dev Dyn. 2011;240:446-456. doi:10.1002/dvdy.22526
Liebling M, Forouhar AS, Gharib M, Fraser SE, Dickinson ME. Four-dimensional cardiac imaging in living embryos via postacquisition synchronization of nongated slice sequences. J Biomed Opt. 2005;10:054001-0540010.
Crocker, J. C. Http://www.Physics.Emory.Edu/faculty/weeks//idl. 1999.

Auteurs

Nabid Salehin (N)

Department of Bioengineering, University of Texas at Arlington, Arlington, Texas, USA.

Tanveer Teranikar (T)

Department of Bioengineering, University of Texas at Arlington, Arlington, Texas, USA.

Juhyun Lee (J)

Department of Bioengineering, University of Texas at Arlington, Arlington, Texas, USA.

Cheng-Jen Chuong (CJ)

Department of Bioengineering, University of Texas at Arlington, Arlington, Texas, USA.

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