Zebrafish as a high throughput model for organ preservation and transplantation research.

cardiac graft cryobiology partial freezing solid organ preservation zebrafish

Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
10 2023
Historique:
revised: 15 08 2023
received: 13 01 2023
accepted: 24 08 2023
medline: 19 9 2023
pubmed: 18 9 2023
entrez: 18 9 2023
Statut: ppublish

Résumé

Despite decades of effort, the preservation of complex organs for transplantation remains a significant barrier that exacerbates the organ shortage crisis. Progress in organ preservation research is significantly hindered by suboptimal research tools that force investigators to sacrifice translatability over throughput. For instance, simple model systems, such as single cell monolayers or co-cultures, lack native tissue structure and functional assessment, while mammalian whole organs are complex systems with confounding variables not compatible with high-throughput experimentation. In response, diverse fields and industries have bridged this experimental gap through the development of rich and robust resources for the use of zebrafish as a model organism. Through this study, we aim to demonstrate the value zebrafish pose for the fields of solid organ preservation and transplantation, especially with respect to experimental transplantation efforts. A wide array of methods were customized and validated for preservation-specific experimentation utilizing zebrafish, including the development of assays at multiple developmental stages (larvae and adult), methods for loading and unloading preservation agents, and the development of viability scores to quantify functional outcomes. Using this platform, the largest and most comprehensive screen of cryoprotectant agents (CPAs) was performed to determine their toxicity and efficiency at preserving complex organ systems using a high subzero approach called partial freezing (i.e., storage in the frozen state at -10°C). As a result, adult zebrafish cardiac function was successfully preserved after 5 days of partial freezing storage. In combination, the methods and techniques developed have the potential to drive and accelerate research in the fields of solid organ preservation and transplantation.

Identifiants

pubmed: 37718489
doi: 10.1096/fj.202300076R
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23187

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL157803
Pays : United States
Organisme : NIH HHS
ID : R24 OD031955
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL164749
Pays : United States

Commentaires et corrections

Type : ErratumIn

Informations de copyright

© 2023 The Authors. The FASEB Journal published by Wiley Periodicals LLC on behalf of Federation of American Societies for Experimental Biology.

Références

Pinezich M, Vunjak-Novakovic G. Bioengineering approaches to organ preservation ex vivo. Exp Biol Med (Maywood). 2019;244(8):630-645.
Kilic A, Emani S, Sai-Sudhakar CB, Higgins RS, Whitson BA. Donor selection in heart transplantation. J Thorac Dis. 2014;6(8):1097-1104.
Giwa S, Lewis JK, Alvarez L, et al. The promise of organ and tissue preservation to transform medicine. Nat Biotechnol. 2017;35(6):530-542.
Chiu-Lam A, Staples E, Pepine CJ, Rinaldi C. Perfusion, cryopreservation, and nanowarming of whole hearts using colloidally stable magnetic cryopreservation agent solutions. Sci Adv. 2021;7(2):eabe3005.
Hackmann M, English RA, Kizer KW, eds. Realizing the Promise of Equity in the Organ Transplantation System. The National Academies Press; 2022.
Taylor MJ, Weegman BP, Baicu SC, Giwa SE. New approaches to cryopreservation of cells, tissues, and organs. Transfus Med Hemother. 2019;46(3):197-215.
Finger EB, Bischof JC. Cryopreservation by vitrification: a promising approach for transplant organ banking. Curr Opin Organ Transplant. 2018;23(3):353-360.
de Vries RJ, Tessier SN, Banik PD, et al. Subzero non-frozen preservation of human livers in the supercooled state. Nat Protoc. 2020;15(6):2024-2040.
Powell-Palm MJ, Charwat V, Charrez B, Siemons B, Healy KE, Rubinsky B. Isochoric supercooled preservation and revival of human cardiac microtissues. Commun Biol. 2021;4(1):1118.
Tessier SN, de Vries RJ, Pendexter CA, et al. Partial freezing of rat livers extends preservation time by 5-fold. Nat Commun. 2022;13(1):4008.
Howe K, Clark MD, Torroja CF, et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature. 2013;496(7446):498-503.
Kokel D, Bryan J, Laggner C, et al. Rapid behavior-based identification of neuroactive small molecules in the zebrafish. Nat Chem Biol. 2010;6(3):231-237.
Gonzalez-Rosa JM. Zebrafish models of cardiac disease: from fortuitous mutants to precision medicine. Circ Res. 2022;130(12):1803-1826.
Cornet C, Calzolari S, Miñana-Prieto R, et al. ZeGlobalTox: an innovative approach to address organ drug toxicity using zebrafish. Int J Mol Sci. 2017;18(4):864.
Dyballa S, Miñana R, Rubio-Brotons M, et al. Comparison of zebrafish larvae and hiPSC cardiomyocytes for predicting drug induced cardiotoxicity in humans. Toxicol Sci. 2019;171:283-295.
Pieperhoff S, Wilson KS, Baily J, et al. Heart on a plate: histological and functional assessment of isolated adult zebrafish hearts maintained in culture. PloS One. 2014;9(5):e96771.
Genge CE, Lin E, Lee L, et al. The zebrafish heart as a model of mammalian cardiac function. Rev Physiol Biochem Pharmacol. 2016;171:99-136.
Cronin S, Pendexter CA, Kimura S, et al. Partial Freezing: Subzero Whole Liver Preservation in the Presence of Ice. American Journal of Transplantation. Wiley; 2019.
Liu XH, Zhang T, Rawson DM. Effect of cooling rate and partial removal of yolk on the chilling injury in zebrafish (Danio rerio) embryos. Theriogenology. 2001;55(8):1719-1731.
Patton EE, Zon LI, Langenau DM. Zebrafish disease models in drug discovery: from preclinical modelling to clinical trials. Nat Rev Drug Discov. 2021;20(8):611-628.
Pegg DE. Principles of cryopreservation. Methods Mol Biol. 2007;368:39-57.
Tessier SN, Weng L, Moyo WD, et al. Effect of ice nucleation and cryoprotectants during high subzero-preservation in endothelialized microchannels. ACS Biomater Sci Eng. 2018;4(8):3006-3015.
Norris MM, Aksan A, Sugimachi K, Toner M. 3-O-methyl-D-glucose improves desiccation tolerance of keratinocytes. Tissue Eng. 2006;12(7):1873-1879.
Usta OB, Kim Y, Ozer S, et al. Supercooling as a viable non-freezing cell preservation method of rat hepatocytes. PloS One. 2013;8(7):e69334.
Warner RM, Ampo E, Nelson D, Benson JD, Eroglu A, Higgins AZ. Rapid quantification of multi-cryoprotectant toxicity using an automated liquid handling method. Cryobiology. 2021;98:219-232.
Lin C, Zhang T, Rawson DM. Cryopreservation of zebrafish (Danio rerio) blastomeres by controlled slow cooling. Cryo Lett. 2009;30(2):132-141.
Zhan L, Li MG, Hays T, Bischof J. Cryopreservation method for Drosophila melanogaster embryos. Nat Commun. 2021;12(1):2412.
Khosla K, Kangas J, Liu Y, et al. Cryopreservation and laser nanowarming of zebrafish embryos followed by hatching and spawning. Adv Biosyst. 2020;4(11):e2000138.
Campbell LH, Brockbank KG. Cryopreservation of porcine aortic heart valve leaflet-derived myofibroblasts. Biopreserv Biobank. 2010;8(4):211-217.
Fahy GM. Cryoprotectant toxicity neutralization. Cryobiology. 2010;60(3 Suppl):S45-S53.
Best BP. Cryoprotectant toxicity: facts, issues, and questions. Rejuvenation Res. 2015;18(5):422-436.
Que W, Hu X, Fujino M, et al. Prolonged cold ischemia time in mouse heart transplantation using supercooling preservation. Transplantation. 2020;104(9):1879-1889.
Bruinsma BG, Berendsen TA, Izamis ML, Yeh H, Yarmush ML, Uygun K. Supercooling preservation and transplantation of the rat liver. Nat Protoc. 2015;10(3):484-494.
He JH, Guo SY, Zhu F, et al. A zebrafish phenotypic assay for assessing drug-induced hepatotoxicity. J Pharmacol Toxicol Methods. 2013;67(1):25-32.
Guo S. Using zebrafish to assess the impact of drugs on neural development and function. Expert Opin Drug Discov. 2009;4(7):715-726.
Field HA, Kelley KA, Martell L, Golstein AM, Serluca FC. Analysis of gastrointestinal physiology using a novel intestinal transit assay in zebrafish. Neurogastroenterol Motil. 2009;21(3):304-312.
Pegg DE, Wang L, Vaughan D. Cryopreservation of articular cartilage. Part 3: the liquidus-tracking method. Cryobiology. 2006;52(3):360-368.
Corral A, Balcerzyk M, Parrado-Gallego Á, et al. Assessment of the cryoprotectant concentration inside a bulky organ for cryopreservation using X-ray computed tomography. Cryobiology. 2015;71(3):419-431.
Isbell SA, Fyfe CA, Ammons RLM, Pearson B. Measurement of cryoprotective solvent penetration into intact organ tissues using high-field NMR microimaging. Cryobiology. 1997;35(2):165-172.
Stoyek MR, Quinn TA, Croll RP, Smith FM. Zebrafish heart as a model to study the integrative autonomic control of pacemaker function. Am J Physiol Heart Circ Physiol. 2016;311(3):H676-H688.
Bowley G, Kugler E, Wilkinson R, et al. Zebrafish as a tractable model of human cardiovascular disease. Br J Pharmacol. 2022;179(5):900-917.
Bagdonas AA, Stuckey JH, Piera J, Amer NS, Hoffman BF. Effects of ischemia and hypoxia on the specialized conducting system of the canine heart. Am Heart J. 1961;61(2):206-218.
Senges J, Mizutani T, Pelzer D, Brachmann J, Sonnhof U, Kübler W. Effect of hypoxia on the sinoatrial node, atrium, and atrioventricular node in the rabbit heart. Circ Res. 1979;44(6):856-863.
James TN, Sherf L, Fine G, Morales AR. Comparative ultrastructure of the sinus node in man and dog. Circulation. 1966;34(1):139-163.
Sherf L, James TN, Woods WT. Function of the atrioventricular node considered on the basis of observed histology and fine structure. J Am Coll Cardiol. 1985;5(3):770-780.
Lutz J, Thurmel K, Heemann U. Anti-inflammatory treatment strategies for ischemia/reperfusion injury in transplantation. J Inflamm (Lond). 2010;7:27.
Mandla R, Jung C, Vedantham V. Transcriptional and epigenetic landscape of cardiac pacemaker cells: insights into cellular specialization in the sinoatrial node. Front Physiol. 2021;12:712666.
Iorga B, Neacsu CD, Neiss WF, et al. Micromechanical function of myofibrils isolated from skeletal and cardiac muscles of the zebrafish. J Gen Physiol. 2011;137(3):255-270.
Ostadalova I, Ostadal B, Kolář F, Parratt JR, Wilson S. Tolerance to ischaemia and ischaemic preconditioning in neonatal rat heart. J Mol Cell Cardiol. 1998;30(4):857-865.
Riva E, Hearse DJ. Age-dependent changes in myocardial susceptibility to ischemic injury. Cardioscience. 1993;4(2):85-92.
Spence R, Gerlach G, Lawrence C, Smith C. The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc. 2008;83(1):13-34.

Auteurs

Luciana Da Silveira Cavalcante (L)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Manuela Lopera Higuita (M)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Juan Manuel González-Rosa (JM)

Cardiovascular Research Center, Massachusetts General Hospital Research Institute, Harvard Medical School, Charlestown, Massachusetts, USA.

Beatriz Marques (B)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.

Samantha To (S)

Cardiovascular Research Center, Massachusetts General Hospital Research Institute, Harvard Medical School, Charlestown, Massachusetts, USA.

Casie A Pendexter (CA)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Stephanie E J Cronin (SEJ)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Kaustav Gopinathan (K)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.

Reinier J de Vries (RJ)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Felix Ellett (F)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Korkut Uygun (K)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

David M Langenau (DM)

Molecular Pathology Unit and Cancer Center, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts, USA.

Mehmet Toner (M)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Shannon N Tessier (SN)

Center for Engineering in Medicine and Surgery, Harvard Medical School and Massachusetts General Hospital, Boston, Massachusetts, USA.
Shriners Hospitals for Children - Boston, Boston, Massachusetts, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH