Sex-specific DNA methylation and transcription of zbtb38 and effects of gene–environment interactions on its natural antisense transcript in zebrafish

References

• Sapir Y, Mazer SJ, Holzapfel C. Sex ratio. In: Jørgensen S, Fath B, editors. Encyclopedia of ecology. Oxford: Academic Press; 2008. p. 3243–13. doi: 10.1016/B978-008045405-4.00658-3
   Google Scholar
• Schwanz LE, Georges A. Sexual development and the environment: conclusions from 40 years of theory. Sex Dev. 2021 Sept;15(1–3):7–22. doi: 10.1159/000515221
   PubMed Web of Science ®Google Scholar
• Kendall NW, Quinn TP. Size-selective fishing affects sex ratios and the opportunity for sexual selection in Alaskan sockeye salmon Oncorhynchus nerka. Oikos. 2013 Sept;122(3):411–420. doi: 10.1111/j.1600-0706.2012.20319.x
   Web of Science ®Google Scholar
• Capel B. Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat Rev Genet. 2017 Nov;18(11):675–689. doi: 10.1038/nrg.2017.60
   PubMed Web of Science ®Google Scholar
• Piferrer F. Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems. Phil Trans R Soc B query. 2021 Aug 30;376(1832):20200110.
   PubMed Web of Science ®Google Scholar
• Santos D, Luzio A, Coimbra AM. Zebrafish sex differentiation and gonad development: a review on the impact of environmental factors. Aquat Toxicol. 2017 Oct;191:141–163. doi: 10.1016/j.aquatox.2017.08.005
   PubMed Web of Science ®Google Scholar
• Shao C, Li Q, Chen S, et al. Epigenetic modification and inheritance in sexual reversal of fish. Genome Res. 2014 Apr;24(4):604–615. doi: 10.1101/gr.162172.113
   PubMed Web of Science ®Google Scholar
• Hays GC, Mazaris AD, Schofield G, et al. Population viability at extreme sex-ratio skews produced by temperature-dependent sex determination. Proc Biol Sci. 2017 Feb;284(1848):20162576. doi: 10.1098/rspb.2016.2576
   PubMed Web of Science ®Google Scholar
• Geffroy B, Wedekind C. Effects of global warming on sex ratios in fishes. J Fish Biol. 2020 Sep;97(3):596–606. doi: 10.1111/jfb.14429
   PubMed Web of Science ®Google Scholar
• Pierron F, Lorioux S, Héroin D, et al. Transgenerational epigenetic sex determination: environment experienced by female fish affects offspring sex ratio. Environ Pollut. 2021 May;277:116864.
   PubMed Web of Science ®Google Scholar
• Guirandy N, Gagnaire B, Camilleri V, et al. Multigenerational exposure to gamma radiation affects offspring differently over generations in zebrafish. Aquat Toxicol. 2022 Mar;244:106101.
   PubMed Web of Science ®Google Scholar
• Hagen R, Ortmann S, Elliger A, et al. Evidence for a male-biased sex ratio in the offspring of a large herbivore: the role of environmental conditions in the sex ratio variation. Ecol Evol. 2022 May;12(5):e8938. doi: 10.1002/ece3.8938
   PubMed Web of Science ®Google Scholar
• Wilson CA, High SK, McCluskey BM, et al. Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics. 2014 Nov;198(3):1291–1308. doi: 10.1534/genetics.114.169284
   PubMed Web of Science ®Google Scholar
• Valdivieso A, Ribas L, Monleón-Getino A, et al. Exposure of zebrafish to elevated temperature induces sex ratio shifts and alterations in the testicular epigenome of unexposed offspring. Environ Res. 2020 Jul;186:109601.
   PubMed Web of Science ®Google Scholar
• Navarro-Martín L, Viñas J, Ribas L, et al. DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet. 2011 Dec;7(12):e1002447. doi: 10.1371/journal.pgen.1002447
   PubMed Web of Science ®Google Scholar
• Yang YJ, Wang Y, Li Z, et al. Sequential, divergent, and cooperative requirements of Foxl2a and Foxl2b in ovary development and maintenance of zebrafish. Genetics. 2017 Apr;205(4):1551–1572. doi: 10.1534/genetics.116.199133
   PubMed Web of Science ®Google Scholar
• Ribas L, Vanezis K, Imués MA, et al. Treatment with a DNA methyltransferase inhibitor feminizes zebrafish and induces long-term expression changes in the gonads. Epigenet Chromatin. 2017 Dec;10(1):59. doi: 10.1186/s13072-017-0168-7
   PubMedGoogle Scholar
• Ortega-Recalde O, Day RC, Gemmell NJ, et al. Zebrafish preserve global germline DNA methylation while sex-linked rDNA is amplified and demethylated during feminisation. Nat Commun. 2019 Jul;10(1):3053. doi: 10.1038/s41467-019-10894-7
   PubMedGoogle Scholar
• Skvortsova K, Tarbashevich K, Stehling M, et al. Retention of paternal DNA methylome in the developing zebrafish germline. Nat Commun. 2019 Jul;10(1):3054. doi: 10.1038/s41467-019-10895-6
   PubMedGoogle Scholar
• Pierron F, Heroin D, Daffe G, et al. Genetic and epigenetic interplay allows rapid transgenerational adaptation to metal pollution in zebrafish. Environ Epigenet. 2022 Oct;8(1):dvac022. doi: 10.1093/eep/dvac022
   PubMed Web of Science ®Google Scholar
• Pierron F, Daffe G, Daramy F, et al. Transgenerational endocrine disruptor effects of cadmium in zebrafish and contribution of standing epigenetic variation to adaptation. J Hazard Mater. 2023;455:131579. doi: 10.1016/j.jhazmat.2023.131579
   PubMed Web of Science ®Google Scholar
• Yang Y, Zhou T, Liu Y, et al. Identification of an epigenetically marked locus within the sex determination region of channel catfish. Int J Mol Sci. 2022 May;23(10):5471. doi: 10.3390/ijms23105471
   PubMed Web of Science ®Google Scholar
• Pan N, Wang M, Zhong L, et al. Identification of male-specific SNP markers and development of rapid PCR-based genetic sex identification method in channel catfish (Ictalurus punctatus). Aquaculture. 2022 Jan;547:737535. doi: 10.1016/j.aquaculture.2021.737535
   Web of Science ®Google Scholar
• Marchal C, Defossez PA, Miotto B. Context-dependent CpG methylation directs cell-specific binding of transcription factor ZBTB38. Epigenetics. 2022 Dec;17(13):2122–2143. doi: 10.1080/15592294.2022.2111135
   PubMed Web of Science ®Google Scholar
• Lin YT, Capel B. Cell fate commitment during mammalian sex determination. Curr Opin Genet Dev. 2015 Jun;32:144–152. doi: 10.1016/j.gde.2015.03.003
   PubMed Web of Science ®Google Scholar
• Untergasser A, Nijveen H, Rao X, et al. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W71–4. doi: 10.1093/nar/gkm306
   PubMedGoogle Scholar
• McCurley AT, Callard GV. Characterization of housekeeping genes in zebrafish: male-female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Biol. 2008 Nov;9(1):102. doi: 10.1186/1471-2199-9-102
   PubMedGoogle Scholar
• Ratnu VS, Emami MR, Bredy TW. Genetic and epigenetic factors underlying sex differences in the regulation of gene expression in the brain. J Neurosci Res. 2017 Jan;95(1–2):301–310. doi: 10.1002/jnr.23886
   PubMed Web of Science ®Google Scholar
• Ribas L, Valdivieso A, Díaz N, Piferrer F. Appropriate rearing density in domesticated zebrafish to avoid masculinization: links with the stress response. J Exp Biol. 2017 Mar;220(Pt 6):1056–1064. doi: 10.1242/jeb.167437
   PubMed Web of Science ®Google Scholar
• Hammoud SS, Low DH, Yi C, et al. Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell. 2014 Aug 7;15(2):239–253. doi: 10.1016/j.stem.2014.04.006
   PubMed Web of Science ®Google Scholar
• Piferrer F, Anastasiadi D, Valdivieso A, et al. The model of the conserved epigenetic regulation of sex. Front Genet. 2019 Sep 26;10:857.
   PubMed Web of Science ®Google Scholar
• Héberlé É, Bardet AF. Sensitivity of transcription factors to DNA methylation. Essays Biochem. 2019 Dec 20;63(6):727–741. doi: 10.1042/EBC20190033
   PubMed Web of Science ®Google Scholar
• Zinad HS, Natasya I, Werner A. Natural antisense transcripts at the interface between host genome and mobile genetic elements. Front Microbiol. 2017 Nov;8:2292. doi: 10.3389/fmicb.2017.02292
   PubMed Web of Science ®Google Scholar
• Khorkova O, Stahl J, Joji A, et al. Natural antisense transcripts as drug targets. Front Mol Biosci. 2022 Sep;9:978375.
   PubMed Web of Science ®Google Scholar
• Frías-Lasserre D, Villagra CA. The importance of ncRnas as epigenetic mechanisms in phenotypic variation and organic evolution. Front Microbiol. 2017 Dec;8:2483. doi: 10.3389/fmicb.2017.02483
   PubMed Web of Science ®Google Scholar
• Sarangdhar MA, Chaubey D, Srikakulam N, et al. Parentally inherited long non-coding RNA Cyrano is involved in zebrafish neurodevelopment. Nucleic Acids Res. 2018 Oct;46(18):9726–9735. doi: 10.1093/nar/gky628
   PubMed Web of Science ®Google Scholar
• Martín L, Kamstra JH, Hurem S, et al. Altered non-coding RNA expression profile in F1 progeny 1 year after parental irradiation is linked to adverse effects in zebrafish. Sci Rep. 2021 Feb;11(1):4142. doi: 10.1038/s41598-021-83345-3
   PubMed Web of Science ®Google Scholar
• Skinner MK, Nilsson E, Sadler-Riggleman I, et al. Transgenerational sperm DNA methylation epimutation developmental origins following ancestral vinclozolin exposure. Epigenetics. 2019 Jul;14(7):721–739. doi: 10.1080/15592294.2019.1614417
   PubMed Web of Science ®Google Scholar
• Cheuquemán C, Maldonado R. Non-coding RNAs and chromatin: key epigenetic factors from spermatogenesis to transgenerational inheritance. Biol Res. 2021 Dec;54(1):41. doi: 10.1186/s40659-021-00364-0
   PubMed Web of Science ®Google Scholar
• Ishihara T, Griffith OW, Suzuki S, et al. Placental imprinting of SLC22A3 in the IGF2R imprinted domain is conserved in therian mammals. Epigenet Chromatin. 2022 Aug;15(1):32. doi: 10.1186/s13072-022-00465-4
   PubMed Web of Science ®Google Scholar