Calling the question: what is mammalian transgenerational epigenetic inheritance?

References

• Radford EJ. Exploring the extent and scope of epigenetic inheritance. Nat Rev Endocrinol. 2018;14(6):345–12. doi: 10.1038/s41574-018-0005-5
   PubMed Web of Science ®Google Scholar
• Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293(5532):1089–1093. doi: 10.1126/science.1063443
   PubMed Web of Science ®Google Scholar
• Rotondo JC, Lanzillotti C, Mazziotta C, et al. Epigenetics of male infertility: the role of DNA methylation. Front Cell Dev Biol. 2021;9:689624. doi: 10.3389/fcell.2021.689624
   PubMedGoogle Scholar
• Tahmasbpour Marzouni E, Ilkhani H, Beigi Harchegani A, et al. Epigenetic modifications, a new approach to male infertility etiology: a review. Int J Fertil Steril. 2022;16(1):1–9. doi: 10.22074/IJFS.2021.138499.1032
   PubMed Web of Science ®Google Scholar
• Slyvka Y, Zhang Y, Nowak FV. Epigenetic effects of paternal diet on offspring: emphasis on obesity. Endocrine. 2015;48(1):36–46. doi: 10.1007/s12020-014-0328-5
   PubMed Web of Science ®Google Scholar
• Fallet M, Blanc M, Di Criscio M, et al. Present and future challenges for the investigation of transgenerational epigenetic inheritance. Environ Int. 2023;172:107776. doi: 10.1016/j.envint.2023.107776
   PubMed Web of Science ®Google Scholar
• Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8(4):253–262. doi: 10.1038/nrg2045
   PubMed Web of Science ®Google Scholar
• van Otterdijk SD, Michels KB. Transgenerational epigenetic inheritance in mammals: how good is the evidence? FASEB J Off Publ Fed Am Soc Exp Biol. 2016;30(7):2457–2465. doi: 10.1096/fj.201500083
   PubMed Web of Science ®Google Scholar
• Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008;105(44):17046–17049. doi: 10.1073/pnas.0806560105
   PubMed Web of Science ®Google Scholar
• Blewitt ME, Vickaryous NK, Paldi A, et al. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet. 2006a;2(4):e49. doi: 10.1371/journal.pgen.0020049
   PubMed Web of Science ®Google Scholar
• Dolinoy DC, Weidman JR, Waterland RA, et al. Maternal genistein alters coat color and protects A vy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect. 2006;114(4):567–572. doi: 10.1289/ehp.8700
   PubMed Web of Science ®Google Scholar
• Morgan HD, Sutherland HG, Martin DI, et al. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999;23(3):314–318. doi: 10.1038/15490
   PubMed Web of Science ®Google Scholar
• Anway MD, Cupp AS, Uzumcu M, et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308(5727):1466–1469. doi: 10.1126/science.1108190
   PubMed Web of Science ®Google Scholar
• Roseboom TJ, Painter RC, van Abeelen AFM, et al. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas. 2011;70(2):141–145. doi: 10.1016/j.maturitas.2011.06.017
   PubMed Web of Science ®Google Scholar
• Carone BR, Fauquier L, Habib N, et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell. 2010;143(7):1084–1096. doi: 10.1016/j.cell.2010.12.008
   PubMed Web of Science ®Google Scholar
• Terashima M, Barbour S, Ren J, et al. Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression. Epigenetics. 2015;10(9):861–871. doi: 10.1080/15592294.2015.1075691
   PubMed Web of Science ®Google Scholar
• Ryan DP, Henzel KS, Pearson BL, et al. A paternal methyl donor-rich diet altered cognitive and neural functions in offspring mice. Mol Psychiatry. 2018;23(5):1345–1355. doi: 10.1038/mp.2017.53
   PubMed Web of Science ®Google Scholar
• Wen J, Hong Q, Wang X, et al. The effect of maternal vitamin D deficiency during pregnancy on body fat and adipogenesis in rat offspring. Sci Rep. 2018;8(1):365. doi: 10.1038/s41598-017-18770-4
   PubMedGoogle Scholar
• Ponomarev I, Wang S, Zhang L, et al. Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J Neurosci Off J Soc Neurosci. 2012;32(5):1884–1897. doi: 10.1523/JNEUROSCI.3136-11.2012
   PubMed Web of Science ®Google Scholar
• Govorko D, Bekdash RA, Zhang C, et al. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol Psychiatry. 2012;72(5):378–388. doi: 10.1016/j.biopsych.2012.04.006
   PubMed Web of Science ®Google Scholar
• Caton JS, Crouse MS, McLean KJ, et al. Maternal periconceptual nutrition, early pregnancy, and developmental outcomes in beef cattle. J Anim Sci. 2020;98(12):skaa358. doi: 10.1093/jas/skaa358
   PubMed Web of Science ®Google Scholar
• Muhlhausler BS, Duffield JA, McMillen IC. Increased maternal nutrition stimulates peroxisome proliferator activated receptor-γ, Adiponectin, and leptin messenger ribonucleic acid expression in adipose tissue before birth. Endocrinology. 2007;148(2):878–885. doi: 10.1210/en.2006-1115
   PubMed Web of Science ®Google Scholar
• Sinclair KD, Allegrucci C, Singh R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci. 2007;104(49):19351–19356. doi: 10.1073/pnas.0707258104
   PubMed Web of Science ®Google Scholar
• Leroux S, Gourichon D, Leterrier C, et al. Embryonic environment and transgenerational effects in quail. Genet Sel Evol. 2017;49(1):14. doi: 10.1186/s12711-017-0292-7
   PubMedGoogle Scholar
• Heard E, Martienssen RA. Transgenerational epigenetic inheritance: myths and mechanisms. Cell. 2014;157(1):95–109. doi: 10.1016/j.cell.2014.02.045
   PubMed Web of Science ®Google Scholar
• Martos SN, Tang W, Wang Z. Elusive inheritance: transgenerational effects and epigenetic inheritance in human environmental disease. Prog Biophys Mol Biol. 2015;118(1–2):44–54. doi: 10.1016/j.pbiomolbio.2015.02.011
   PubMed Web of Science ®Google Scholar
• Santilli F, Boskovic A. Mechanisms of transgenerational epigenetic inheritance: lessons from animal model organisms. Curr Opin Genet Dev. 2023;79:102024. doi: 10.1016/j.gde.2023.102024
   PubMed Web of Science ®Google Scholar
• Tuscher JJ, Day JJ. Multigenerational epigenetic inheritance: one step forward, two generations back. Neurobiol Dis. 2019;132:104591. doi: 10.1016/j.nbd.2019.104591
   PubMed Web of Science ®Google Scholar
• Horsthemke B. A critical view on transgenerational epigenetic inheritance in humans. Nat Commun. 2018;9(1):2973. doi: 10.1038/s41467-018-05445-5
   PubMedGoogle Scholar
• Anway MD, Leathers C, Skinner MK. Endocrine Disruptor Vinclozolin Induced Epigenetic Transgenerational Adult-Onset Disease. Endocrinology. 2006;147(12):5515–5523. doi: 10.1210/en.2006-0640
   PubMed Web of Science ®Google Scholar
• Guerrero-Bosagna C, Covert TR, Haque MM, et al. Epigenetic transgenerational inheritance of vinclozolin induced mouse adult onset disease and associated sperm epigenome biomarkers. Reprod Toxicol. 2012;34(4):694–707. doi: 10.1016/j.reprotox.2012.09.005
   PubMed Web of Science ®Google Scholar
• Iqbal K, Tran DA, Li AX, et al. Deleterious effects of endocrine disruptors are corrected in the mammalian germline by epigenome reprogramming. Genome Biol. 2015;16(1):59. doi: 10.1186/s13059-015-0619-z
   PubMedGoogle Scholar
• Nadeau JH. The nature of evidence for and against epigenetic inheritance. Genome Biol. 2015;16(1):137. doi: 10.1186/s13059-015-0709-y
   PubMedGoogle Scholar
• Blake GE, Watson ED. Unravelling the complex mechanisms of transgenerational epigenetic inheritance. Curr Opin Chem Biol. 2016;33:101–107. doi: 10.1016/j.cbpa.2016.06.008
   PubMed Web of Science ®Google Scholar
• Nilsson EE, Sadler-Riggleman I, Skinner MK, et al. Environmentally induced epigenetic transgenerational inheritance of disease. Environ Epigenetics. 2018;4(2). doi: 10.1093/eep/dvy016
   Google Scholar
• Blanco Rodríguez J, Camprubí Sánchez C. Epigenetic Transgenerational Inheritance. Adv Exp Med Biol. 2019;1166:57–74. doi: 10.1007/978-3-030-21664-1_4
   PubMed Web of Science ®Google Scholar
• Wang HD, Allard P. Challenging dogmas: how transgenerational epigenetics reshapes our views on life. J Exp Zool Part Ecol Integr Physiol. 2022;337(1):70–74. doi: 10.1002/jez.2465
   PubMed Web of Science ®Google Scholar
• Braz CU, Taylor T, Namous H, et al. Paternal diet induces transgenerational epigenetic inheritance of DNA methylation signatures and phenotypes in sheep model. PNAS Nexus. 2022;1(2):pgac040. doi: 10.1093/pnasnexus/pgac040
   PubMedGoogle Scholar
• Inawaka K, Kawabe M, Takahashi S, et al. Maternal exposure to anti-androgenic compounds, vinclozolin, flutamide and procymidone, has no effects on spermatogenesis and DNA methylation in male rats of subsequent generations. Toxicol Appl Pharmacol. 2009;237(2):178–187. doi: 10.1016/j.taap.2009.03.004
   PubMed Web of Science ®Google Scholar
• Schneider S, Kaufmann W, Buesen R, et al. Vinclozolin—the lack of a transgenerational effect after oral maternal exposure during organogenesis. Reprod Toxicol. 2008;25(3):352–360. doi: 10.1016/j.reprotox.2008.04.001
   PubMed Web of Science ®Google Scholar
• Nilsson E, Larsen G, Manikkam M, et al. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS One. 2012;7(5):e36129. doi: 10.1371/journal.pone.0036129
   PubMed Web of Science ®Google Scholar
• Brieño-Enríquez MA, García-López J, Cárdenas DB, et al. Exposure to endocrine disruptor induces transgenerational epigenetic deregulation of MicroRNAs in primordial germ cells. PLoS One. 2015;10(4):e0124296. doi: 10.1371/journal.pone.0124296
   PubMed Web of Science ®Google Scholar
• Abraham A, Chakraborty P. A review on sources and health impacts of bisphenol a. Rev Environ Health. 2020;35(2):201–210. doi: 10.1515/reveh-2019-0034
   PubMed Web of Science ®Google Scholar
• Rahman MS, Pang WK, Ryu DY, et al. Multigenerational and transgenerational impact of paternal bisphenol a exposure on male fertility in a mouse model. Hum Reprod. 2020;35(8):1740–1752. doi: 10.1093/humrep/deaa139.
   PubMed Web of Science ®Google Scholar
• Wolstenholme JT, Goldsby JA, Rissman EF. Transgenerational effects of prenatal bisphenol a on social recognition. Horm Behav. 2013;64(5):833–839. doi: 10.1016/j.yhbeh.2013.09.007
   PubMed Web of Science ®Google Scholar
• Franklin TB, Russig H, Weiss IC, et al. Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry. 2010;68(5):408–415. doi: 10.1016/j.biopsych.2010.05.036
   PubMed Web of Science ®Google Scholar
• Dias BG, Ressler KJ. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci. 2014;17(1):89–96. doi: 10.1038/nn.3594
   PubMed Web of Science ®Google Scholar