Optical Elastography for Micropressure Characterization of Zebrafish Embryonic Cardiac Development.
Blood pressure
Cardiac development
Contractile patterns
Optical elastography
Zebrafish embryo
Journal
Annals of biomedical engineering
ISSN: 1573-9686
Titre abrégé: Ann Biomed Eng
Pays: United States
ID NLM: 0361512
Informations de publication
Date de publication:
30 Nov 2023
30 Nov 2023
Historique:
received:
04
07
2023
accepted:
21
11
2023
medline:
1
12
2023
pubmed:
1
12
2023
entrez:
30
11
2023
Statut:
aheadofprint
Résumé
The proper formation of the vertebrate embryonic heart relies on various mechanical forces which determine its form and function. Measuring these forces at the microscale of the embryo is a challenge. We propose a new tool utilizing high-resolution optical elastography and stiffness measurements of surrounding tissues to non-invasively track the changes in the pressure exerted by the heart on the neighboring yolk, as well as changes in contractile patterns during early cardiac growth in-vivo, using the zebrafish embryo as a model system. Cardiac development was characterized every three hours from 24 hours post-fertilization (hpf) to 30 hpf and compared between wildtype fish and those treated with MS-222, a commonly used fish anesthetic that decreases cardiac contractility. Wildtype embryos from 24 to 30 hpf showed an average yolk indentation pressure of 0.32 mmHg to 0.41 mmHg, respectively. MS-222 treated embryos showed an average yolk indentation pressure of 0.22 mmHg to 0.29 mmHg. Yolk indentation pressure between control and treated embryos at 24 hpf and 30 hpf showed a significant difference (p < 0.05). Our method allowed for contractility and pressure evaluation at these early developmental stages, which have not been previously reported in published literature, regardless of sample or imaging modality. This research could lead to a better understanding of heart development and improved diagnostic tools for congenital heart disease.
Identifiants
pubmed: 38036895
doi: 10.1007/s10439-023-03413-9
pii: 10.1007/s10439-023-03413-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Science Foundation
ID : CCSS-1809047
Organisme : National Science Foundation
ID : CAREER-1942518
Organisme : National Science Foundation
ID : IIBR-2223957
Informations de copyright
© 2023. The Author(s) under exclusive licence to Biomedical Engineering Society.
Références
Almeida, A., G. Andrews, D. Jaiswal, and K. Hoshino. The actuation mechanism of 3D printed flexure-based robotic microtweezers. Micromachines (Basel). 10:470, 2019. https://doi.org/10.3390/mi10070470 .
doi: 10.3390/mi10070470
pubmed: 31337134
Bakkers, J. Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc Res. 91:279–288, 2011. https://doi.org/10.1093/cvr/cvr098 .
doi: 10.1093/cvr/cvr098
pubmed: 21602174
pmcid: 3125074
Brown, D. R., L. A. Samsa, L. Qian, and J. Liu. Advances in the study of heart development and disease using zebrafish. J Cardiovasc Dev Dis. 3:13, 2016. https://doi.org/10.3390/jcdd3020013 .
doi: 10.3390/jcdd3020013
pubmed: 27335817
pmcid: 4913704
Cairelli, A. G., R.W.-Y. Chow, J. Vermot, and C. H. Yap. Fluid mechanics of the zebrafish embryonic heart trabeculation. PLOS Comput Biol.18:e1010142, 2022. https://doi.org/10.1371/journal.pcbi.1010142 .
doi: 10.1371/journal.pcbi.1010142
pubmed: 35666714
pmcid: 9203006
Denvir, M. A., C. S. Tucker, and J. J. Mullins. Systolic and diastolic ventricular function in zebrafish embryos: Influence of norepenephrine, MS-222 and temperature. BMC Biotechnol. 8:21, 2008. https://doi.org/10.1186/1472-6750-8-21 .
doi: 10.1186/1472-6750-8-21
pubmed: 18304347
pmcid: 2291041
Foo, Y. Y., S. Pant, H. S. Tay, N. Imangali, N. Chen, C. Winkler, and C. H. Yap. 4D modelling of fluid mechanics in the zebrafish embryonic heart. Biomech Model Mechanobiol. 19:221–232, 2020. https://doi.org/10.1007/s10237-019-01205-6 .
doi: 10.1007/s10237-019-01205-6
pubmed: 31446522
Félix, L. M., A. Luzio, M. Themudo, L. Antunes, M. Matos, A. M. Coimbra, and A. M. Valentim. MS-222 short exposure induces developmental and behavioural alterations in zebrafish embryos. Reprod Toxicol. 81:122–131, 2018. https://doi.org/10.1016/j.reprotox.2018.07.086 .
doi: 10.1016/j.reprotox.2018.07.086
pubmed: 30053429
Gendernalik, A., B. Zebhi, N. Ahuja, D. Garrity, and D. Bark. In vivo pressurization of the zebrafish embryonic heart as a tool to characterize tissue properties during development. Ann Biomed Eng. 2020. https://doi.org/10.1007/s10439-020-02619-5 .
doi: 10.1007/s10439-020-02619-5
pubmed: 32959136
Hsu, J. J., V. Vedula, K. I. Baek, C. Chen, J. Chen, M. I. Chou, J. Lam, S. Subhedar, J. Wang, Y. Ding, C.-C. Chang, J. Lee, L. L. Demer, Y. Tintut, A. L. Marsden, and T. K. Hsiai. Contractile and hemodynamic forces coordinate Notch1b-mediated outflow tract valve formation. JCI Insight.4:e124460, 2019. https://doi.org/10.1172/jci.insight.124460 .
doi: 10.1172/jci.insight.124460
pmcid: 6542601
Hu, N., D. Sedmera, H. J. Yost, and E. B. Clark. Structure and function of the developing zebrafish heart. Anat Rec. 260:148–157, 2000. https://doi.org/10.1002/1097-0185(20001001)260:2%3c148::AID-AR50%3e3.0.CO;2-X .
doi: 10.1002/1097-0185(20001001)260:2<148::AID-AR50>3.0.CO;2-X
pubmed: 10993952
Jaiswal, D., N. Cowley, Z. Bian, G. Zheng, K. P. Claffey, and K. Hoshino. Stiffness analysis of 3D spheroids using microtweezers. PLOS ONE.12:e0188346, 2017. https://doi.org/10.1371/journal.pone.0188346 .
doi: 10.1371/journal.pone.0188346
pubmed: 29166651
pmcid: 5699838
Jaiswal, D., Z. Moscato, Y. Tomizawa, K. P. Claffey, and K. Hoshino. Elastography of multicellular spheroids using 3D light microscopy. Biomed Opt Express. 10:2409–2418, 2019. https://doi.org/10.1364/BOE.10.002409 .
doi: 10.1364/BOE.10.002409
pubmed: 31143496
pmcid: 6524572
Jaiswal, D., M. D. Tang-Schomer, D. Sood, D. L. Kaplan, and K. Hoshino. Nondestructive, label-free characterization of mechanical microheterogeneity in biomimetic materials. ACS Biomater Sci Eng. 4:3259–3267, 2018. https://doi.org/10.1021/acsbiomaterials.8b00286 .
doi: 10.1021/acsbiomaterials.8b00286
pubmed: 33435062
Keller, B. B., W. J. Kowalski, J. P. Tinney, K. Tobita, and N. Hu. Validating the paradigm that biomechanical forces regulate embryonic cardiovascular morphogenesis and are fundamental in the etiology of congenital heart disease. J Cardiovasc Dev Dis. 7:23, 2020. https://doi.org/10.3390/jcdd7020023 .
doi: 10.3390/jcdd7020023
pubmed: 32545681
pmcid: 7344498
Kimmel, C. B., W. W. Ballard, S. R. Kimmel, B. Ullmann, and T. F. Schilling. Stages of embryonic development of the zebrafish. Dev Dyn. 203:253–310, 1995. https://doi.org/10.1002/aja.1002030302 .
doi: 10.1002/aja.1002030302
pubmed: 8589427
Kopp, R., T. Schwerte, and B. Pelster. Cardiac performance in the zebrafish breakdance mutant. J Exp Biol. 208:2123–2134, 2005. https://doi.org/10.1242/jeb.01620 .
doi: 10.1242/jeb.01620
pubmed: 15914656
Lekka, M. Discrimination between normal and cancerous cells using AFM. BioNanoSci. 6:65–80, 2016. https://doi.org/10.1007/s12668-016-0191-3 .
doi: 10.1007/s12668-016-0191-3
Lindsey, S. E., J. T. Butcher, and H. C. Yalcin. Mechanical regulation of cardiac development. Front Physiol. 2014. https://doi.org/10.3389/fphys.2014.00318 .
doi: 10.3389/fphys.2014.00318
pubmed: 25191277
pmcid: 4140306
Malone, M. H., N. Sciaky, L. Stalheim, K. M. Hahn, E. Linney, and G. L. Johnson. Laser-scanning velocimetry: a confocal microscopy method for quantitative measurement of cardiovascular performance in zebrafish embryos and larvae. BMC Biotechnol. 7:40, 2007. https://doi.org/10.1186/1472-6750-7-40 .
doi: 10.1186/1472-6750-7-40
pubmed: 17623073
pmcid: 1955438
Matthews, M., and Z. M. Varga. Anesthesia and euthanasia in zebrafish. ILAR J. 53:192–204, 2012. https://doi.org/10.1093/ilar.53.2.192 .
doi: 10.1093/ilar.53.2.192
pubmed: 23382350
Muntean, B. S., C. M. Horvat, J. H. Behler, W. A. AbouAlaiwi, A. M. Nauli, F. E. Williams, and S. M. Nauli. A comparative study of embedded and anesthetized zebrafish in vivo on myocardiac calcium oscillation and heart muscle contraction. Front Pharmacol. 2010. https://doi.org/10.3389/fphar.2010.00139 .
doi: 10.3389/fphar.2010.00139
pubmed: 21833178
pmcid: 3153013
Plodinec, M., M. Loparic, C. A. Monnier, E. C. Obermann, R. Zanetti-Dallenbach, P. Oertle, J. T. Hyotyla, U. Aebi, M. Bentires-Alj, R. Y. H. Lim, and C.-A. Schoenenberger. The nanomechanical signature of breast cancer. Nat Nanotechnol. 7:757–765, 2012. https://doi.org/10.1038/nnano.2012.167 .
doi: 10.1038/nnano.2012.167
pubmed: 23085644
Popov, V. L. Rigorous Treatment of Contact Problems – Hertzian Contact. In: Contact Mechanics and Friction: Physical Principles and Applications, edited by V. L. Popov. Berlin: Springer, 2010, pp. 55–70.
doi: 10.1007/978-3-642-10803-7_5
Salehin, N., T. Teranikar, J. Lee, and C.-J. Chuong. Ventricular anisotropic deformation and contractile function of the developing heart of zebrafish in vivo. Dev Dyn. 252:247–262, 2023. https://doi.org/10.1002/dvdy.536 .
doi: 10.1002/dvdy.536
pubmed: 36057940
Salehin, N., C. Villarreal, T. Teranikar, B. Dubansky, J. Lee, and C.-J. Chuong. Assessing pressure-volume relationship in developing heart of zebrafish in-vivo. Ann Biomed Eng. 49:2080–2093, 2021. https://doi.org/10.1007/s10439-021-02731-0 .
doi: 10.1007/s10439-021-02731-0
pubmed: 33532949
Sharifi, A., A. Gendernalik, D. Garrity, and D. Bark. Valveless pumping behavior of the simulated embryonic heart tube as a function of contractile patterns and myocardial stiffness. Biomech Model Mechanobiol. 20:2001–2012, 2021. https://doi.org/10.1007/s10237-021-01489-7 .
doi: 10.1007/s10237-021-01489-7
pubmed: 34297252
Sidhwani, P., and D. Yelon. Fluid forces shape the embryonic heart: insights from zebrafish. Curr Top Dev Biol. 132:395–416, 2019. https://doi.org/10.1016/bs.ctdb.2018.12.009 .
doi: 10.1016/bs.ctdb.2018.12.009
pubmed: 30797515
pmcid: 6394863
Tomizawa, Y., D. F. Daggett, G. Zheng, and K. Hoshino. Light microscopy-based elastography for the mechanical characterization of zebrafish somitogenesis. J Biophoton.16:e202200238, 2023. https://doi.org/10.1002/jbio.202200238 .
doi: 10.1002/jbio.202200238
Tomizawa, Y., K. Dixit, D. Daggett, and K. Hoshino. Biocompatible cantilevers for mechanical characterization of zebrafish embryos using image analysis. Sensors. 19:1506, 2019. https://doi.org/10.3390/s19071506 .
doi: 10.3390/s19071506
pubmed: 30925721
pmcid: 6479902
Xu, X., S. E. Meiler, T. P. Zhong, M. Mohideen, D. A. Crossley, W. W. Burggren, and M. C. Fishman. Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin. Nat Genet. 30:205–209, 2002. https://doi.org/10.1038/ng816 .
doi: 10.1038/ng816
pubmed: 11788825
Yalcin, H. C., A. Amindari, J. T. Butcher, A. Althani, and M. Yacoub. Heart function and hemodynamic analysis for zebrafish embryos. Dev Dyn. 246:868–880, 2017. https://doi.org/10.1002/dvdy.24497 .
doi: 10.1002/dvdy.24497
pubmed: 28249360
Zhang, R., A. A. Gashev, D. C. Zawieja, and M. J. Davis. Length-tension relationships of small arteries, veins, and lymphatics from the rat mesenteric microcirculation. Am J Physiol. 292:H1943–H1952, 2007. https://doi.org/10.1152/ajpheart.01000.2005 .
doi: 10.1152/ajpheart.01000.2005
Zhang, H., and K.-K. Liu. Optical tweezers for single cells. J R Soc Interface. 5:671–690, 2008. https://doi.org/10.1098/rsif.2008.0052 .
doi: 10.1098/rsif.2008.0052
pubmed: 18381254
pmcid: 2408388