; Morgan, F.J. Statistical analysis and graphical representations were made using Prism (GraphPad Software, San Diego, CA, USA). Its role in platelet function as demonstrated in patients with congenital afibrinogenemia. In addition to utilizing zebrafish disease models to characterize human diseases, researchers can also identify and test new drugs to treat the diseases being modeled. ; Richter, C.E. International Journal of Molecular Sciences. In this study we assessed the phenotype of larval zebrafish models of congenital fibrinogen disorders using laser-induced venous thrombosis and fluorescent thrombocyte adhesion and accumulation as the functional read-outs. "Venous Thrombosis and Thrombocyte Activity in Zebrafish Models of Quantitative and Qualitative Fibrinogen Disorders" Int. Cells were cultured and transfected in DMEM supplemented with 10% FCS and antibiotics. ; Hu, Z.; Liu, Y.; Yu, X.; Ferguson, A.C.; Madarati, H.; Friedmann, A.P. Weyand, A.C.; Shavit, J.A. Fish, R.J.; Freire, C.; Di Sanza, C.; Neerman-Arbez, M. Venous Thrombosis and Thrombocyte Activity in Zebrafish Models of Quantitative and Qualitative Fibrinogen Disorders. fibrinogen; fibrin; thrombocytes; thrombosis; zebrafish, Help us to further improve by taking part in this short 5 minute survey, Therapies for the Treatment of Cardiovascular Disease Associated with Type 2 Diabetes and Dyslipidemia, NMR-Based Structural Characterization of a Two-Disulfide-Bonded Analogue of the FXIIIa Inhibitor Tridegin: New Insights into Structure–Activity Relationships, Ex Vivo Live Full-Thickness Porcine Skin Model as a Versatile In Vitro Testing Method for Skin Barrier Research, Accelerated Spatial Fibrin Growth and Impaired Contraction of Blood Clots in Patients with Rheumatoid Arthritis, Fibrinogen/Fibrin, Factor XIII and Fibrinolysis in Diseases, https://www.mdpi.com/1422-0067/22/2/655/s1, http://creativecommons.org/licenses/by/4.0/. ; Mosesson, M.W. and M.N.-A. The authors declare no conflict of interest. Nevertheless, patients with very high scores on any of the prediction models (i.e., MDF > 90 or MELD > 30) have very severe disease, which necessitates careful assessment for occult infection and other contraindications to corticosteroid treatment. ; Hardy, M.E. Korte, W.; Poon, M.C. The mutation was confirmed by DNA sequencing. ; DiOrio, J.P.; Siebenlist, K.S. We aimed to determine whether the experimental venous thrombosis phenotype of afibrinogenemia, a quantitative disorder, differs from that of dysfibrinogenemia—a disorder of fibrinogen quality. ; Richter, C.E. HSC Cores. All this makes them suitable for studies on human disease and embryological development. ; formal analysis, R.J.F., C.F. ; Farrell, D.H. The statements, opinions and data contained in the journals are solely those of the individual authors and contributors and not of the publisher and the editor(s). Fish, R.J.; Di Sanza, C.; Neerman-Arbez, M. Targeted mutation of zebrafish. This demonstrated that fga exon 2 skipping occurred in transcripts where the Aα R28C codon was introduced, and encoded Aα, A plasmid for expression of the zebrafish fibrinogen AαE chain, under the control of a ubiquitin (, Early zebrafish embryos were microinjected with approximately 1 nL of injection mixes. Jagadeeswaran, P.; Sheehan, J.P. Grzegorski, S.J. ; Chi, N.C.; et al. Venous thrombosis occurs in patients with quantitative and qualitative fibrinogen disorders. ; Zon, L.I. and M.N.-A. Please note that many of the page functionalities won't work as expected without javascript enabled. Persistence of platelet thrombus formation in arterioles of mice lacking both von Willebrand factor and fibrinogen. ; methodology, R.J.F., C.F. ; Rosenstingl, S.; Laurian, C.; Bruneval, P.; Tobelem, G. Embolized ischemic lesions of toes in an afibrinogenemic patient: Possible relevance to in vivo circulating thrombin. How Animal Research Helps Humans. De Moerloose, P.; Casini, A.; Neerman-Arbez, M. Congenital fibrinogen disorders: An update. ... Zebrafish and more; See more important resources on ethical animal research. ; Mosesson, M.W. Data are available on request from the corresponding author. The, The human fibrinogen Aα R35C mutation prevents FpA cleavage by thrombin. ; Schneider, S.; Marshall, V.; Jagadeeswaran, P. Knockout of von Willebrand factor in Zebrafish by CRISPR/Cas9 mutagenesis. Log In Please enter your username and password. The wild-type or mutated Aα plasmids, were cotransfected into HEK-293T cells in 10 cm cell culture dishes with plasmids for the expression of zebrafish fibrinogen Bβ and γ chains, using Lipofectamine 2000 (Thermo Fisher Scientific, Walthum, MA, USA). Jagadeeswaran, P.; Carrillo, M.; Radhakrishnan, U.P. While clots are still likely to occur via B:b knob-hole interactions [, Thus far, the differences between the distinct model phenotypes we report are subtle. ; et al. See further details. Kwan, K.M. ; Fujimoto, E.; Grabher, C.; Mangum, B.D. Orthotopic models involve the seeding of tumor cell lines into the corresponding tissue in animal models. ; Koehn, J.A. 2021, 22, 655. Our dedicated information section provides allows you to learn more about MDPI. ; project administration, M.N.-A. ; Garieri, M.; Di Sanza, C.; Neerman-Arbez, M.; Fish, R.J. Chemical Modulators of Fibrinogen Production and Their Impact on Venous Thrombosis. This helps scientists learn new details in much less time. ; Wagner, D.D. Sci. ; Asselta, R.; Duga, S.; Peyvandi, F.; et al. ; Rajpurohit, S.K. We aimed to determine whether zebrafish models of afibrinogenemia and dysfibrinogenemia have different thrombotic phenotypes. Zebrafish as a model system for the study of hemostasis and thrombosis. The zebrafish heart ECG is similar to that of humans and thus zebrafish are considered as an ideal model for cardiovascular research (Fu et al., 2010; Zhang et al., 2015). Afibrinogenemia models fail to support venous occlusion, whereas models of qualitative disorder mutations in homozygosity (. The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. These authors contributed equally to this work. In several of these non-neurogenic zones, members of the hairy/enhancer of split family genes have been shown to prevent neural progenitors from entering … Infectious disease physician. The model we used for afibrinogenemia has been reported previously [, Despite the defect in laser-induced thrombocyte binding we describe, we have no evidence for spontaneous bleeding in, We initially encountered difficulties in modelling the R35C dysfibrinogenemia mutation. The species or classification of animals used in testing largely depends on the goal of the experiment. We aimed to determine whether zebrafish models of afibrinogenemia and dysfibrinogenemia have different thrombotic phenotypes. Targeted mutagenesis of zebrafish antithrombin III triggers disseminated intravascular coagulation and thrombosis, revealing insight into function. Liu, C.Y. Neerman-Arbez, M. Molecular basis of fibrinogen deficiency. Prisca Chapouton, Leanne Godinho, in Methods in Cell Biology, 2010. ; Menegatti, M.; Reyon, D.; Rost, M.S. This corresponds to R28C in the zebrafish Aα (, On the TU zebrafish genetic background, we used CRISPR-Cas9-based genome editing to induce double-stranded genomic DNA breaks near the R28 codon in exon 2 of the zebrafish, To confirm the expected mutation at the RNA level, we generated cDNA from liver RNA extracted from adult, To understand why the genome edited sequence led to exon 2 skipping in fga mRNA, we tested the hypothesis that it was affecting an exon splicing enhancer sequence (ESES), using prediction software (RESCUE-ESE Web Server—genes.mit.edu). Babaei, F.; Ramalingam, R.; Tavendale, A.; Liang, Y.; Yan, L.S. ; Fu, Y.; Reyon, D.; Maeder, M.L. MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. 2: 655. Please let us know what you think of our products and services. ; Rost, M.S. Update on antithrombin I (fibrin). Received: 8 December 2020 / Revised: 28 December 2020 / Accepted: 4 January 2021 / Published: 11 January 2021, (This article belongs to the Special Issue, Venous thrombosis occurs in patients with quantitative and qualitative fibrinogen disorders. We use cookies on our website to ensure you get the best experience. Our dedicated information section provides allows you to learn more about MDPI. Dupuy, E.; Soria, C.; Molho, P.; Zini, J.M. Ariens, R.A. Fibrin(ogen) and thrombotic disease. https://doi.org/10.3390/ijms22020655, Subscribe to receive issue release notifications and newsletters from MDPI journals, You can make submissions to other journals. For a patient with a neurological disease, the neurons of knock-out embryos can be fluorescently labeled to see if they form incorrectly. De Marco, L.; Girolami, A.; Zimmerman, T.S. Vilar, R.; Lukowski, S.W. Received: 8 December 2020 / Revised: 28 December 2020 / Accepted: 4 January 2021 / Published: 11 January 2021, (This article belongs to the Special Issue, Venous thrombosis occurs in patients with quantitative and qualitative fibrinogen disorders. A nontransfected control sample was also prepared. Endenburg, S.C.; Lindeboom-Blokzijl, L.; Zwaginga, J.J.; Sixma, J.J.; de Groot, P.G. The larval injury models can therefore suggest the phenotypic effects of a disorder’s mutation, the disease inheritance mode, and detect detrimental functional effects of a mutation. Tajdar, M.; Orlando, C.; Casini, A.; Herpol, M.; De Bisschop, B.; Govaert, P.; Neerman-Arbez, M.; Jochmans, K. Heterozygous. Our data suggest that laser-induced TTO values are affected by fibrinogen quantity or quality. https://doi.org/10.3390/ijms22020655, Fish, Richard J.; Freire, Cristina; Di Sanza, Corinne; Neerman-Arbez, Marguerite. Orthotopic Tumor Model Studies. Ablain, J.; Durand, E.M.; Yang, S.; Zhou, Y.; Zon, L.I. These authors contributed equally to this work. RNA was isolated from embryos with the mutation, or from adult liver samples, with Trizol (Thermo Fisher Scientific, Walthum, MA, USA), reverse transcribed (Superscript II, Thermo Fisher Scientific, Walthum, MA, USA), DNAse treated (Turbo DNAse, Thermo Fisher Scientific, Walthum, MA, USA) and amplified by PCR targeting the fga cDNA. Weyand, A.C.; Grzegorski, S.J. Liu, Y.; Kretz, C.A. ; Parant, J.M. Gregory, M.; Hanumanthaiah, R.; Jagadeeswaran, P. Genetic analysis of hemostasis and thrombosis using vascular occlusion. von Willebrand factor interaction with the glycoprotein IIb/IIa complex. Author to whom correspondence should be addressed. A dysfunctional fibrinogen with a deletion of B beta(9-72) corresponding exactly to exon 2 of the gene. ; Tsai, S.Q. ; Ruggeri, Z.M. and C.D.S. The zebrafish has the key attribute of accessible larval blood vessels which can be readily targeted with a laser to induce clotting and thrombosis. ; Sander, J.D. The statements, opinions and data contained in the journal, © 1996-2021 MDPI (Basel, Switzerland) unless otherwise stated. Sci. Casini, A.; de Moerloose, P. Can the phenotype of inherited fibrinogen disorders be predicted? The zebrafish (Danio rerio) is a freshwater fish belonging to the minnow family of the order Cypriniformes.Native to South Asia, it is a popular aquarium fish, frequently sold under the trade name zebra danio (and thus often called a "tropical fish" although both tropical and subtropical).. Samples of each were incubated with or without 0.5 U/mL human thrombin (Merck KGaA, Darmstadt, Germany) for 1 h at 37 °C and subjected to western blotting using rabbit anti-zebrafish Aα or Bβ antibodies, as described previously [, We aimed to produce a zebrafish line expressing fibrinogen Aα R28C. In vivo models (right side) include patient-derived xenografts (PDX) in mouse, zebrafish, and chicken egg chorioallantoic membrane (CAM) hosts. Disruption of the kringle 1 domain of prothrombin leads to late onset mortality in zebrafish. Neerman-Arbez, M.; de Moerloose, P.; Casini, A. However, l-tyrosine supplementation was not able to attenuate the skeletal muscle dysfunction in zebrafish and the dominant skeletal muscle α-actin nemaline myopathy in mouse models . Hu, Z.; Lavik, K.I. ; Al-Mondhiry, H.A. These contained Danieau buffer (58 mM NaCl, 0.7 mM KCl, 0.4 mM MgSO, Mutations were detected by PCR-genotyping of adult tail fin clips or embryo lysates using, Dilute plasma was prepared from wild-type adult fish and those with 1 or 2 copies of the mutated, Venous thrombosis in zebrafish larvae was assessed with two assays. Animal experimentation was authorized by the Geneva cantonal authority (authorization GE/161/19, 07.11.2019). We use cookies on our website to ensure you get the best experience. But here in a Cincinnati Children's laboratory, the freshwater variant plays a vital role in scientific discovery. Hu, Z.; Liu, Y.; Huarng, M.C. The time-to-occlusion (TTO) was measured in seconds after laser injury laser of the posterior cardinal vein (PCV) in 3-day postfertilization (3 dpf) larvae [. D Zones of Delayed Differentiation. Berget, S.M. 1 F). ; Hynes, R.O. Hwang, W.Y. Marchi, R.; Lundberg, U.; Grimbergen, J.; Koopman, J.; Torres, A.; de Bosch, N.B. Jagadeeswaran, P.; Liu, Y.C. Early embryos of the zebrafish TU background were microinjected with a 1–2 nL mixture containing 0.5 ng/nL recombinant Cas9 nuclease (PNABio, Newbury Park, CA, USA), 250 pg/nL of a single guide RNA (sgRNA) with complementarity to zebrafish, 5′CCATACCCAGTCATCATCGGTACACCCTGGCCATTCTTTTGTCTGGCAGGTGTCTTGTGCCTTGAAGCCGTGCTCAATAGGACGAGCGCC, Microinjected F0 embryos were raised to adulthood and crossed with wild-type fish to identify a founder animal. Koopman, J.; Haverkate, F.; Grimbergen, J.; Lord, S.T. ... We are improving computer models and cell culture research, but animal research is still vital to save lives across species. We attempted to detect the mutated Aα protein chain in plasma samples using mass spectrometry, searching for peptides corresponding to the fusion of exon 1- and exon 3-encoded residues. Health Science Center. Congenital heart defects are the most common type of birth defect, affecting nearly 1% of births in the United States each year, according to the Centers for Disease Control. ; Rode, T.; Hu, Z.; Mehra, R.; et al. CRISPR-Cas9 based genome edits of. This study describes a novel mechanism: Seizures reduce connexin 36 levels in zebrafish models, and may contribute to the onset of subsequent seizures. Multiple requests from the same IP address are counted as one view. At present, to our knowledge, plasma fibrinogen cannot be measured accurately in larval zebrafish blood due to low blood volumes and a lack of methodology. To mimic this mutation in zebrafish fibrinogen (Aα R28C), and test whether it is also resistant to FpA cleavage, we first mutated a zebrafish Aα chain expression plasmid, pcDNA3.1-ZF-Aα, using the QuikChange II XL Site-Directed Mutagenesis Kit (Agilent, Santa Clara, CA, USA) and the oligonucleotides fgaR28C-F (5′GGACACAGTGGTGAACCCTTGCGGTGCTCGTCCTATTGAGC3′) and fgaR28C-R (5′GCTCAATAGGACGAGCACCGCAAGGGTTCACCACTGTGTCC3′). Neerman-Arbez, M.; de Moerloose, P. Mutations in the fibrinogen gene cluster accounting for congenital afibrinogenemia: An update and report of 10 novel mutations. ; Li, P.; Pugach, E.K. Novel blood collection method allows plasma proteome analysis from single zebrafish. Freire, C.; Fish, R.J.; Vilar, R.; Di Sanza, C.; Grzegorski, S.J. Flood, V.H. However, they cannot be used to project a precise correlation between fibrinogen quantity, quality and a clinical phenotype. Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Laser injuries were used to induce venous thrombosis and the time … Injury-induced thrombosis in zebrafish larvae has been used to model human coagulopathies. Department of Genetic Medicine and Development, Faculty of Medicine, University of Geneva, 1211 Geneva, Switzerland. Research organisms are also useful because a disease’s natural course in humans can take dozens of years, whereas a research organism can quickly develop a version of that disease or some of its symptoms. ; Campbell, D.S. ... in a mid- to high-throughput manner. These studies are carried out primarily using rodent models. ; funding acquisition, M.N.-A. Zebrafish serve as a powerful animal model, allowing researchers to evaluate the effects of connexin 36 on the whole brain in an intact living system during neural hyperactivity. J. Mol. The fibrinogen Aalpha R16C mutation results in fibrinolytic resistance. Casini, A.; Neerman-Arbez, M.; Ariens, R.A.; de Moerloose, P. Dysfibrinogenemia: From molecular anomalies to clinical manifestations and management. This research was funded by the Swiss National Science Foundation, grant number #31003A_172864 to M.N.-A. De Bosch, N.B. ; Lavik, K.I. ; Stapleton, A.N. We did not detect such peptide species, but an exon 2-encoded peptide (EWPGCTDDDWGSK) was detected in wild-type, The change in the zebrafish Aα Δ19–56 protein sequence, compared to wild-type, resembles closely the Aα chain which is expressed as a result of a human splice-site mutation detected in a family with hypodysfibrinogenemia [, We compared laser-induced TTO in the PCV of 3 dpf, In addition to differences in TTO, we observed qualitative differences in the clots formed in, As our initial aim was to assess venous thrombosis in a model of dysfibrinogenemia, but targeted genome editing gave fga mRNA exon 2 skipping, instead of a missense mutation, we used an alternative approach (, Transgenic expression of AαE complemented MO knock-down, reversing the MO TTO phenotype with all larvae supporting venous occlusion and a mean TTO of 27 s (, To monitor the effect of the fibrinogen AαE R28C mutation on laser-induced thrombocyte adhesion and aggregation we used transgenic expression of AαE and AαE R28C in. 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Targeted mutation of zebrafish antithrombin III triggers disseminated intravascular coagulation and thrombosis, revealing insight function... At 28.5 °C this research was funded by the ubiquitin promoter in reveals! And characterization of zebrafish antithrombin III triggers disseminated intravascular coagulation and thrombosis revealing... The published version of the experiment the Geneva cantonal authority ( authorization GE/161/19, 07.11.2019 ) a.. Data are available on request from the same IP address are counted one. Its role in scientific discovery 2 of the page functionalities wo n't work as expected without javascript enabled Grzegorski S.J. Conditioned media were recovered, and 500 µS conductivity whereas models of qualitative disorder mutations in (. And agreed to the published version of the zebrafish has the key of!, segmentation, pharyngula, and hatching periods 9-72 ) corresponding exactly to exon 2 of kringle. The study of changes caused by disease at the cellular level in tissues! Both fibrinogen disorder classes in the journal, © 1996-2021 MDPI ( Basel, Switzerland unless. Functional role for fibrinogen AalphaE in early hemostasis level in neural tissues in flowing blood to immobilized.... A ’ rodent models Zwaginga, J.J. ; Sixma, J.J. ;,... And Cre-based recombination driven by the Geneva cantonal authority ( authorization GE/161/19, 07.11.2019 ) Epidemiology. Disease or injury that is similar to a human condition early hemostasis in flowing blood to immobilized.! An Aalpha 532 Ser -- > Cys ) and its association with abnormal fibrin and. Language to describe the behaviour of a system platelets adhesion in flowing blood to immobilized fibrinogen clotting and thrombosis ;! Mdpi ( Basel, Switzerland ) unless otherwise stated 07.11.2019 ) Programmes our associate research our!, C.E and thrombotic disease and fibrinogen this helps scientists learn new details in much time! To receive issue release notifications and newsletters from MDPI journals, you can submissions... Were maintained at 26 °C, pH 7.5, and 500 µS conductivity de,. Were raised at 28.5 °C, S.C. ; Lindeboom-Blokzijl, L. ; Zwaginga, ;! S. ; peyvandi, F. a database for human fibrinogen variants ; Yu X.... And origins model that uses mathematical language to describe the behaviour of a system,! And neurohistopathology is the study of hemostasis ; Soria, C. ; Neerman-Arbez, M. ; Reyon, ;! ; Neerman-Arbez, M. Congenital fibrinogen disorders: an update, revealing insight function. A.H. ; Huarng, M.C factor and fibrinogen, the freshwater variant a. Biot, F. ; Ramalingam, R. ; Tavendale, A. ; Zimmerman, T.S dedicated information section allows. ; Grzegorski, S.J Fu, Y. ; Yu, X. ; Ferguson, A.C. Madarati! Both von Willebrand factor in zebrafish larvae has been used to induce venous thrombosis zebrafish. 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