Intergenerational and Transgenerational Epigenetic Inheritance in Animals

Overview

Journal Nat Cell Biol

Specialty Cell Biology

Date 2019 Jan 4

PMID 30602724

Citations 190

Authors

Marcos Francisco Perez

Ben Lehner

Affiliations

Soon will be listed here.

Abstract

Animals transmit not only DNA but also other molecules, such as RNA, proteins and metabolites, to their progeny via gametes. It is currently unclear to what extent these molecules convey information between generations and whether this information changes according to their physiological state and environment. Here, we review recent work on the molecular mechanisms by which 'epigenetic' information is transmitted between generations over different timescales, and the importance of this information for development and physiology.

Citing Articles

New insights into how parental worms protect their offspring.

Zeng C, Miska E Cell Res. 2025; .

PMID: 40082682 DOI: 10.1038/s41422-025-01094-8.

EBAX-1/ZSWIM8 destabilizes miRNAs, resulting in transgenerational inheritance of a predatory trait.

Quiobe S, Kalirad A, Roseler W, Witte H, Wang Y, Rodelsperger C Sci Adv. 2025; 11(11):eadu0875.

PMID: 40073139 PMC: 11900880. DOI: 10.1126/sciadv.adu0875.

Epigenetic signatures of intergenerational exposure to violence in three generations of Syrian refugees.

Mulligan C, Quinn E, Hamadmad D, Dutton C, Nevell L, Binder A Sci Rep. 2025; 15(1):5945.

PMID: 40016245 PMC: 11868390. DOI: 10.1038/s41598-025-89818-z.

Adult killifish exposure to crude oil perturbs embryonic gene expression and larval morphology in first- and second-generation offspring.

Park J, Hess C, Adams C, Brown C, Rocke D, Aeppli C bioRxiv. 2025; .

PMID: 39990372 PMC: 11844404. DOI: 10.1101/2025.02.10.637481.

Inter- and Transgenerational Effects of In Ovo Stimulation with Bioactive Compounds on Cecal Tonsils and Cecal Mucosa Transcriptomes in a Chicken Model.

Ibrahim M, Bednarczyk M, Stadnicka K, Grochowska E Int J Mol Sci. 2025; 26(3).

PMID: 39940944 PMC: 11817890. DOI: 10.3390/ijms26031174.

References

Conrad D, Keebler J, DePristo M, Lindsay S, Zhang Y, Casals F . Variation in genome-wide mutation rates within and between human families. Nat Genet. 2011; 43(7):712-4. PMC: 3322360. DOI: 10.1038/ng.862. View

Skinner M . What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol. 2007; 25(1):2-6. PMC: 2249610. DOI: 10.1016/j.reprotox.2007.09.001. View

Heard E, Martienssen R . Transgenerational epigenetic inheritance: myths and mechanisms. Cell. 2014; 157(1):95-109. PMC: 4020004. DOI: 10.1016/j.cell.2014.02.045. View

Deans C, Maggert K . What do you mean, "epigenetic"?. Genetics. 2015; 199(4):887-96. PMC: 4391566. DOI: 10.1534/genetics.114.173492. View

Ptashne M . Epigenetics: core misconcept. Proc Natl Acad Sci U S A. 2013; 110(18):7101-3. PMC: 3645541. DOI: 10.1073/pnas.1305399110. View

Rando O . Daddy issues: paternal effects on phenotype. Cell. 2012; 151(4):702-708. PMC: 3564497. DOI: 10.1016/j.cell.2012.10.020. View

Rando O, Verstrepen K . Timescales of genetic and epigenetic inheritance. Cell. 2007; 128(4):655-68. DOI: 10.1016/j.cell.2007.01.023. View

Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S . CRISPR provides acquired resistance against viruses in prokaryotes. Science. 2007; 315(5819):1709-12. DOI: 10.1126/science.1138140. View

Ashe A, Sapetschnig A, Weick E, Mitchell J, Bagijn M, Cording A . piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell. 2012; 150(1):88-99. PMC: 3464430. DOI: 10.1016/j.cell.2012.06.018. View

10.

Bagijn M, Goldstein L, Sapetschnig A, Weick E, Bouasker S, Lehrbach N . Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science. 2012; 337(6094):574-578. PMC: 3951736. DOI: 10.1126/science.1220952. View

11.

Shirayama M, Seth M, Lee H, Gu W, Ishidate T, Conte Jr D . piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell. 2012; 150(1):65-77. PMC: 3597741. DOI: 10.1016/j.cell.2012.06.015. View

12.

Luteijn M, van Bergeijk P, Kaaij L, Almeida M, Roovers E, Berezikov E . Extremely stable Piwi-induced gene silencing in Caenorhabditis elegans. EMBO J. 2012; 31(16):3422-30. PMC: 3419935. DOI: 10.1038/emboj.2012.213. View

13.

Fridmann-Sirkis Y, Stern S, Elgart M, Galili M, Zeisel A, Shental N . Delayed development induced by toxicity to the host can be inherited by a bacterial-dependent, transgenerational effect. Front Genet. 2014; 5:27. PMC: 3933808. DOI: 10.3389/fgene.2014.00027. View

14.

Dietz D, LaPlant Q, Watts E, Hodes G, Russo S, Feng J . Paternal transmission of stress-induced pathologies. Biol Psychiatry. 2011; 70(5):408-14. PMC: 3217197. DOI: 10.1016/j.biopsych.2011.05.005. View

15.

Rando O, Simmons R . I'm eating for two: parental dietary effects on offspring metabolism. Cell. 2015; 161(1):93-105. PMC: 4465102. DOI: 10.1016/j.cell.2015.02.021. View

16.

Pembrey M, Bygren L, Kaati G, Edvinsson S, Northstone K, Sjostrom M . Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006; 14(2):159-66. DOI: 10.1038/sj.ejhg.5201538. View

17.

Veenendaal M, Painter R, de Rooij S, Bossuyt P, van der Post J, Gluckman P . Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG. 2013; 120(5):548-53. DOI: 10.1111/1471-0528.12136. View

18.

Zambrano E, Martinez-Samayoa P, Bautista C, Deas M, Guillen L, Rodriguez-Gonzalez G . Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J Physiol. 2005; 566(Pt 1):225-36. PMC: 1464716. DOI: 10.1113/jphysiol.2005.086462. View

19.

Anderson L, Riffle L, Wilson R, Travlos G, Lubomirski M, Alvord W . Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition. 2006; 22(3):327-31. DOI: 10.1016/j.nut.2005.09.006. View

20.

Jimenez-Chillaron J, Isganaitis E, Charalambous M, Gesta S, Pentinat-Pelegrin T, Faucette R . Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes. 2008; 58(2):460-8. PMC: 2628621. DOI: 10.2337/db08-0490. View