• This record comes from PubMed

Ancient Sturgeons Possess Effective DNA Repair Mechanisms: Influence of Model Genotoxicants on Embryo Development of Sterlet, Acipenser ruthenus

. 2020 Dec 22 ; 22 (1) : . [epub] 20201222

Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
GAČR 19-11140Y Czech Science Foundation
LM2018099 Ministry of Education, Youth and Sports of the Czech Republic
CZ.02.1.01/0.0/0.0/16_025/0007370 Ministry of Education, Youth and Sports of the Czech Republic
86652036 RVO CEP Register
CZ.1.05/1.1.00/02.0109 ERDF

DNA damage caused by exogenous or endogenous factors is a common challenge for developing fish embryos. DNA damage repair (DDR) pathways help organisms minimize adverse effects of DNA alterations. In terms of DNA repair mechanisms, sturgeons represent a particularly interesting model due to their exceptional genome plasticity. Sterlet (Acipenser ruthenus) is a relatively small species of sturgeon. The goal of this study was to assess the sensitivity of sterlet embryos to model genotoxicants (camptothecin, etoposide, and benzo[a]pyrene), and to assess DDR responses. We assessed the effects of genotoxicants on embryo survival, hatching rate, DNA fragmentation, gene expression, and phosphorylation of H2AX and ATM kinase. Exposure of sterlet embryos to 1 µM benzo[a]pyrene induced low levels of DNA damage accompanied by ATM phosphorylation and xpc gene expression. Conversely, 20 µM etoposide exposure induced DNA damage without activation of known DDR pathways. Effects of 10 nM camptothecin on embryo development were stage-specific, with early stages, before gastrulation, being most sensitive. Overall, this study provides foundational information for future investigation of sterlet DDR pathways.

See more in PubMed

Tubbs A., Nussenzweig A. Endogenous DNA damage as a source of genomic instability in cancer. Cell. 2017;168:644–656. doi: 10.1016/j.cell.2017.01.002. PubMed DOI PMC

Eisen J.A., Hanawalt P.C. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat. Res. 1999;435:171–213. doi: 10.1016/S0921-8777(99)00050-6. PubMed DOI PMC

Kienzler A., Bony S., Devaux A. DNA repair activity in fish and interest in ecotoxicology: A review. Aquat. Toxicol. 2013;134–135:47–56. doi: 10.1016/j.aquatox.2013.03.005. PubMed DOI

Cayuela M.L., Claes K.B.M., Ferreira M.G., Henriques C.M., van Eeden F., Varga M., Vierstraete J., Mione M.C. The zebrafish as an emerging model to study DNA damage in aging, cancer and other diseases. Front. Cell Dev. Biol. 2018;6:178. doi: 10.3389/fcell.2018.00178. PubMed DOI PMC

Podhorecka M., Skladanowski A., Bozko P. H2AX Phosphorylation: Its role in DNA damage response and cancer therapy. J. Nucleic Acids. 2010;2010 doi: 10.4061/2010/920161. PubMed DOI PMC

Savic V., Yin B., Maas N.L., Bredemeyer A.L., Carpenter A.C., Helmink B.A., Yang-Iott K.S., Sleckman B.P., Bassing C.H. Formation of dynamic gamma-H2AX domains along broken DNA strands is distinctly regulated by ATM and MDC1 and dependent upon H2AX densities in chromatin. Mol. Cell. 2009;34:298–310. doi: 10.1016/j.molcel.2009.04.012. PubMed DOI PMC

Maréchal A., Zou L. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb. Perspect. Biol. 2013;5 doi: 10.1101/cshperspect.a012716. PubMed DOI PMC

Bakkenist C.J., Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 2003;421:499–506. doi: 10.1038/nature01368. PubMed DOI

Fernandez-Diez C., Gonzalez-Rojo S., Lombo M., Herraez M.P. Tolerance to paternal genotoxic damage promotes survival during embryo development in zebrafish (Danio rerio) Biol. Open. 2018;7 doi: 10.1242/bio.030130. PubMed DOI PMC

Mirza-Aghazadeh-Attari M., Mohammadzadeh A., Yousefi B., Mihanfar A., Karimian A., Majidinia M. 53BP1: A key player of DNA damage response with critical functions in cancer. DNA Repair. 2019;73:110–119. doi: 10.1016/j.dnarep.2018.11.008. PubMed DOI

Soltani T., Safahieh A., Zolgharnain H., Matroodi S. Interactions of oxidative DNA damage and CYP1A gene expression with the liver enzymes in Klunzinger’s mullet exposed to benzo[a]pyrene. Toxicol. Rep. 2019;6:1097–1103. doi: 10.1016/j.toxrep.2019.10.013. PubMed DOI PMC

Corrales J., Fang X., Thornton C., Mei W., Barbazuk W.B., Duke M., Scheffler B.E., Willett K.L. Effects on specific promoter DNA methylation in zebrafish embryos and larvae following benzo[a]pyrene exposure. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2014;163:37–46. doi: 10.1016/j.cbpc.2014.02.005. PubMed DOI PMC

Weigt S., Huebler N., Strecker R., Braunbeck T., Broschard T.H. Zebrafish (Danio rerio) embryos as a model for testing proteratogens. Toxicology. 2011;281:25–36. doi: 10.1016/j.tox.2011.01.004. PubMed DOI

Gunz D., Hess M.T., Naegeli H. Recognition of DNA adducts by human nucleotide excision repair. Evidence for a thermodynamic probing mechanism. J. Biol. Chem. 1996;271:25089–25098. doi: 10.1074/jbc.271.41.25089. PubMed DOI

Wang J.C. DNA topoisomerases. Annu. Rev. Biochem. 1996;65:635–692. doi: 10.1146/annurev.bi.65.070196.003223. PubMed DOI

Karapetian M., Tsikarishvili S., Kulikova N., Kurdadze A., Zaalishvili G. Genotoxic effects of topoisomerase poisoning and PARP inhibition on zebrafish embryos. DNA Repair. 2020;87:102772. doi: 10.1016/j.dnarep.2019.102772. PubMed DOI

Chambers R.C., Davis D.D., Habeck E.A., Roy N.K., Wirgin I. Toxic effects of PCB126 and TCDD on shortnose sturgeon and Atlantic sturgeon. Environ. Toxicol. Chem. 2012;31:2324–2337. doi: 10.1002/etc.1953. PubMed DOI PMC

Havelka M., Bytyutskyy D., Symonova R., Rab P., Flajshans M. The second highest chromosome count among vertebrates is observed in cultured sturgeon and is associated with genome plasticity. Genet. Sel. Evol. 2016;48:12. doi: 10.1186/s12711-016-0194-0. PubMed DOI PMC

Bemis W.E., Findeis E.K., Grande L. An overview of Acipenseriformes. Environ. Biol. Fishes. 1997;48:25–71. doi: 10.1023/A:1007370213924. DOI

Vasil’eva E.D., Vasil’ev V.P., Ponomareva E.N., Lapukhin Y.A. Triple hybrids obtained by artificial hybridization of the Russian sturgeon Acipenser gueldenstaedtii with the hybrid of the starred sturgeon A. stellatus and the great sturgeon A. huso (Acipenseridae): The kind of inheritance of some morphological characters and fertility of the parental hybrid form. J. Ichthyol. 2010;50:605–617. doi: 10.1134/s0032945210080059. DOI

Gille D.A., Famula T.R., May B.P., Schreier A.D. Evidence for a maternal origin of spontaneous autopolyploidy in cultured white sturgeon (Acipenser transmontanus) Aquaculture. 2015;435:467–474. doi: 10.1016/j.aquaculture.2014.10.002. DOI

Van Eenennaam J.P., Fiske A.J., Leal M.J., Cooley-Rieders C., Todgham A.E., Conte F.S., Schreier A.D. Mechanical shock during egg de-adhesion and post-ovulatory ageing contribute to spontaneous autopolyploidy in white sturgeon culture (Acipenser transmontanus) Aquaculture. 2020;515:734530. doi: 10.1016/j.aquaculture.2019.734530. DOI

Kermi C., Lo Furno E., Maiorano D. Regulation of DNA replication in early embryonic cleavages. Genes. 2017;8:42. doi: 10.3390/genes8010042. PubMed DOI PMC

Park C., Lee S.Y., Kim D., Nam Y. Embryonic development of Siberian sturgeon Acipenser baerii under hatchery conditions: An image guide with embryological descriptions. Fish. Aquat. Sci. 2013;16:15–23. doi: 10.5657/FAS.2013.0015. DOI

Pocherniaieva K., Güralp H., Saito T., Pšenička M., Tichopád T., Janko K., Kašpar V. The timing and characterization of maternal to zygote transition and mid-blastula transition in sterlet Acipenser ruthenus and A. ruthenus x Acipenser gueldenstaedtii Hybrid. Turkish J. Fish. Aquat. Sci. 2019;19:167–174. doi: 10.4194/1303-2712-v19_2_09. DOI

Ikegami R., Hunter P., Yager T.D. Developmental activation of the capability to undergo checkpoint-induced apoptosis in the early zebrafish embryo. Dev. Biol. 1999;209:409–433. doi: 10.1006/dbio.1999.9243. PubMed DOI

Šrut M., Štambuk A., Bourdineaud J.-P., Klobučar G.I.V. Zebrafish genome instability after exposure to model genotoxicants. Ecotoxicology. 2015;24:887–902. doi: 10.1007/s10646-015-1432-x. PubMed DOI

Lin Y.C., Wu C.Y., Hu C.H., Pai T.W., Chen Y.R., Wang W.D. Integrated hypoxia signaling and oxidative stress in developmental neurotoxicity of Benzo[a]Pyrene in zebrafish embryos. Antioxidants. 2020;9:731. doi: 10.3390/antiox9080731. PubMed DOI PMC

Gao D., Lin J., Ou K., Chen Y., Li H., Dai Q., Yu Z., Zuo Z., Wang C. Embryonic exposure to benzo(a)pyrene inhibits reproductive capability in adult female zebrafish and correlation with DNA methylation. Environ. Pollut. 2018;240:403–411. doi: 10.1016/j.envpol.2018.04.139. PubMed DOI

Zhao Y., Wang X., Lin X., Zhao S., Lin J. Comparative developmental toxicity of eight typical organic pollutants to red sea bream (Pagrosomus major) embryos and larvae. Environ. Sci. Pollut. Res. Int. 2017;24:9067–9078. doi: 10.1007/s11356-016-6282-4. PubMed DOI

Le Bihanic F., Di Bucchianico S., Karlsson H.L., Dreij K. In vivo micronucleus screening in zebrafish by flow cytometry. Mutagenesis. 2016;31:643–653. doi: 10.1093/mutage/gew032. PubMed DOI

Kovacs R., Bakos K., Urbanyi B., Kovesi J., Gazsi G., Csepeli A., Appl A.J., Bencsik D., Csenki Z., Horvath A. Acute and sub-chronic toxicity of four cytostatic drugs in zebrafish. Environ. Sci. Pollut. Res. Int. 2016;23:14718–14729. doi: 10.1007/s11356-015-5036-z. PubMed DOI

Muslimovic A., Nystrom S., Gao Y., Hammarsten O. Numerical analysis of etoposide induced DNA breaks. PLoS ONE. 2009;4:e5859. doi: 10.1371/annotation/290cebfd-d5dc-4bd2-99b4-f4cf0be6c838. PubMed DOI PMC

Gemkow M.J., Dichter J., Arndt-Jovin D.J. Developmental regulation of DNA-topoisomerases during Drosophila embryogenesis. Exp. Cell Res. 2001;262:114–121. doi: 10.1006/excr.2000.5084. PubMed DOI

Tanaka T., Huang X., Halicka H.D., Zhao H., Traganos F., Albino A.P., Dai W., Darzynkiewicz Z. Cytometry of ATM activation and histone H2AX phosphorylation to estimate extent of DNA damage induced by exogenous agents. Cytometry A. 2007;71:648–661. doi: 10.1002/cyto.a.20426. PubMed DOI PMC

Kurose A., Tanaka T., Huang X., Traganos F., Dai W., Darzynkiewicz Z. Effects of hydroxyurea and aphidicolin on phosphorylation of ataxia telangiectasia mutated on Ser 1981 and histone H2AX on Ser 139 in relation to cell cycle phase and induction of apoptosis. Cytometry A. 2006;69:212–221. doi: 10.1002/cyto.a.20241. PubMed DOI

Ginsburg A.S., Dettlaff T.A. The Russian Sturgeon Acipenser Güldenstädti. Part I. Gametes and early development up to time of hatching. In: Dettlaff T.A., Vassetzky S.G., editors. Animal Species for Developmental Studies. Springer; Boston, MA, USA: 1991. pp. 15–65.

Kosmehl T., Hallare A.V., Braunbeck T., Hollert H. DNA damage induced by genotoxicants in zebrafish (Danio rerio) embryos after contact exposure to freeze-dried sediment and sediment extracts from Laguna Lake (The Philippines) as measured by the comet assay. Mutat. Res. 2008;650:1–14. doi: 10.1016/j.mrgentox.2007.09.009. PubMed DOI

Jaroudi S., SenGupta S. DNA repair in mammalian embryos. Mutat. Res. 2007;635:53–77. doi: 10.1016/j.mrrev.2006.09.002. PubMed DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...