Transgenerational Epigenetic Inheritance of Traumatic Experience in Mammals

. 2023 Jan 01 ; 14 (1) : . [epub] 20230101

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36672861

In recent years, we have seen an increasing amount of evidence pointing to the existence of a non-genetic heredity of the effects of events such as separation from parents, threat to life, or other traumatising experiences such as famine. This heredity is often mediated by epigenetic regulations of gene expression and may be transferred even across several generations. In this review, we focus on studies which involve transgenerational epigenetic inheritance (TEI), with a short detour to intergenerational studies focused on the inheritance of trauma or stressful experiences. The reviewed studies show a plethora of universal changes which stress exposure initiates on multiple levels of organisation ranging from hormonal production and the hypothalamic-pituitary-adrenal (HPA) axis modulation all the way to cognition, behaviour, or propensity to certain psychiatric or metabolic disorders. This review will also provide an overview of relevant methodology and difficulties linked to implementation of epigenetic studies. A better understanding of these processes may help us elucidate the evolutionary pathways which are at work in the course of emergence of the diseases and disorders associated with exposure to trauma, either direct or in a previous generation.

Zobrazit více v PubMed

Mattei A.L., Bailly N., Meissner A. DNA methylation: A historical perspective. Trends Genet. 2022;38:676–707. doi: 10.1016/j.tig.2022.03.010. PubMed DOI

Waddington C.H. The Epigenotype. 1942. Int. J. Epidemiol. 2012;41:10–13. doi: 10.1093/ije/dyr184. PubMed DOI

Newman S.A., Forgacs G., Müller G.B. Before programs: The physical origination of multicellular forms. Int. J. Dev. Biol. 2006;50:289–299. doi: 10.1387/ijdb.052049sn. PubMed DOI

Brink R.A. Paramutation. Annu. Rev. Genet. 1973;7:129–152. doi: 10.1146/annurev.ge.07.120173.001021. PubMed DOI

Jablonka E., Lamb M. Epigenetic Inheritance and Evolution: The Lamarckian Dimension. Oxford University Press; Oxford, UK: 1995.

Markoš A., Švorcová J. Epigenetic Processes and the Evolution of Life. Taylor and Francis; Abingdon, UK: CRC Press; Boca Raton, FL, USA: 2019.

Schmitz R.J., Ecker J.R. Epigenetic and epigenomic variation in Arabidopsis thaliana. Trends Plant Sci. 2012;17:149–154. doi: 10.1016/j.tplants.2012.01.001. PubMed DOI PMC

Verhoeven K.J.F., Jansen J.J., van Dijk P.J., Biere A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010;185:1108–1118. doi: 10.1111/j.1469-8137.2009.03121.x. PubMed DOI

Cubas P., Vincent C., Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 1999;401:157–161. doi: 10.1038/43657. PubMed DOI

Yu R., Wang X., Moazed D. Epigenetic inheritance mediated by coupling of RNAi and histone H3K9 methylation. Nature. 2018;558:615–619. doi: 10.1038/s41586-018-0239-3. PubMed DOI PMC

Seong K.-H., Li D., Shimizu H., Nakamura R., Ishii S. Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell. 2011;145:1049–1061. doi: 10.1016/j.cell.2011.05.029. PubMed DOI

Bantignies F., Grimaud C., Lavrov S., Gabut M., Cavalli G. Inheritance of polycomb-dependent chromosomal interactions in Drosophila. Genes Dev. 2003;17:2406–2420. doi: 10.1101/gad.269503. PubMed DOI PMC

Greer E.L., Maures T.J., Ucar D., Hauswirth A.G., Mancini E., Lim J.P., Benayoun B.A., Shi Y., Brunet A. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature. 2011;479:365–371. doi: 10.1038/nature10572. PubMed DOI PMC

Rechavi O., Houri-Ze’evi L., Anava S., Goh W.S.S., Kerk S.Y., Hannon G.J., Hobert O. Starvation-Induced Transgenerational Inheritance of Small RNAs in C. elegans. Cell. 2014;158:277–287. doi: 10.1016/j.cell.2014.06.020. PubMed DOI PMC

Greer E.L., Beese-Sims S.E., Brookes E., Spadafora R., Zhu Y., Rothbart S.B., Aristizábal-Corrales D., Chen S., Badeaux A.I., Jin Q., et al. A histone methylation network regulates transgenerational epigenetic memory in C. elegans. Cell Rep. 2014;7:113–126. doi: 10.1016/j.celrep.2014.02.044. PubMed DOI PMC

Schwartz-Orbach L., Zhang C., Sidoli S., Amin R., Kaur D., Zhebrun A., Ni J., Gu S.G. Caenorhabditis elegans nuclear RNAi factor SET-32 deposits the transgenerational histone modification, H3K23me3. Elife. 2020;9:e54309. doi: 10.7554/eLife.54309. PubMed DOI PMC

Morgan H.D., Sutherland H., Martin D.I., Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 1999;23:314–318. doi: 10.1038/15490. PubMed DOI

Waterland R.A., Jirtle R.L. Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation. Mol. Cell. Biol. 2003;23:5293–5300. doi: 10.1128/MCB.23.15.5293-5300.2003. PubMed DOI PMC

Cropley J.E., Suter C.M., Beckman K.B., Martin D.I.K. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc. Natl. Acad. Sci. USA. 2006;103:17308–17312. doi: 10.1073/pnas.0607090103. PubMed DOI PMC

Blewitt M., Vickaryous N.K., Paldi A., Koseki H., Whitelaw E. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet. 2006;2:e49. doi: 10.1371/journal.pgen.0020049. PubMed DOI PMC

Wolff G.L. Influence of maternal phenotype on metabolic differentiation of agouti locus mutants in the mouse. Genetics. 1978;88:529–539. doi: 10.1093/genetics/88.3.529. PubMed DOI PMC

Flood W.D., Ruvinsky A. Alternative splicing and expressivity of the Axin(Fu) allele in mice. Heredity. 2001;87:146–152. doi: 10.1046/j.1365-2540.2001.00868.x. PubMed DOI

Waterland R.A., Dolinoy D.C., Lin J.-R., Smith C.A., Shi X., Tahiliani K.G. Maternal Methyl Supplements Increase Offspring DNA methylation at Axin Fused. Genesis. 2006;44:401–406. doi: 10.1002/dvg.20230. PubMed DOI

Bertozzi T.M., Ferguson-Smith A.C. Metastable epialleles and their contribution to epigenetic inheritance in mammals. Semin. Cell Dev. Biol. 2020;97:93–105. doi: 10.1016/j.semcdb.2019.08.002. PubMed DOI

Weyrich A., Benz S., Karl S., Jeschek M., Jewgenow K., Fickel J. Paternal heat exposure causes DNA methylation and gene expression changes of Stat3 in Wild guinea pig sons. Ecol. Evol. 2016;6:2657–2666. doi: 10.1002/ece3.1993. PubMed DOI PMC

Rosenberg T., Marco A., Kisliouk T., Haron A., Shinder D., Druyan S., Meiri N. Embryonic heat conditioning in chicks induces transgenerational heat/immunological resilience via methylation on regulatory elements. FASEB J. 2022;36:e22406. doi: 10.1096/fj.202101948R. PubMed DOI

Lillycrop K.A., Phillips E.S., Jackson A.A., Hanson M.A., Burdge G.C. Dietary Protein Restriction of Pregnant Rats Induces and Folic Acid Supplementation Prevents Epigenetic Modification of Hepatic Gene Expression in the Offspring. J. Nutr. 2005;135:1382–1386. doi: 10.1093/jn/135.6.1382. PubMed DOI

Dunn G.A., Bale T.L. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology. 2011;152:2228–2236. doi: 10.1210/en.2010-1461. PubMed DOI PMC

Ghoshal K., Li X., Datta J., Bai S., Pogribny I., Pogribny M., Huang Y., Young D., Jacob S.T. A Folate- and Methyl-Deficient Diet Alters the Expression of DNA Methyltransferases and Methyl CpG Binding Proteins Involved in Epigenetic Gene Silencing in Livers of F344 Rats1. J. Nutr. 2006;136:1522–1527. doi: 10.1093/jn/136.6.1522. PubMed DOI PMC

Pembrey M.E., Bygren L.O., Kaati G., Edvinsson S., Northstone K., Sjöström M., Golding J., the ALSPAC Study Team Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 2006;14:159–166. doi: 10.1038/sj.ejhg.5201538. PubMed DOI

Vassoler F.M., Johnson N.L., Byrnes E.M. Female adolescent exposure to cannabinoids causes transgenerational effects on morphine sensitization in female offspring in the absence of in utero exposure. J. Psychopharmacol. 2013;27:1015–1022. doi: 10.1177/0269881113503504. PubMed DOI PMC

Gangisetty O., Chaudhary S., Palagani A., Sarkar D.K. Transgenerational inheritance of fetal alcohol effects on proopiomelanocortin gene expression and methylation, cortisol response to stress, and anxiety-like behaviors in offspring for three generations in rats: Evidence for male germline transmission. PLoS ONE. 2022;17:e0263340. doi: 10.1371/journal.pone.0263340. PubMed DOI PMC

Uzumcu M., Suzuki H., Skinner M.K. Effect of the anti-androgenic endocrine disruptor vinclozolin on embryonic testis cord formation and postnatal testis development and function. Reprod. Toxicol. 2004;18:765–774. doi: 10.1016/j.reprotox.2004.05.008. PubMed DOI

Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Toxicology: Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466–1469. doi: 10.1126/science.1108190. PubMed DOI PMC

Anway M.D., Leathers C., Skinner M.K. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology. 2006;147:5515–5523. doi: 10.1210/en.2006-0640. PubMed DOI PMC

Crews D., Gore A.C., Hsu T.S., Dangleben M., Spinetta N.L., Schallert T., Anway M.K., Skinner M.D. Transgenerational epigenetic imprints on mate preference. Proc. Natl. Acad. Sci. USA. 2007;104:5942–5946. doi: 10.1073/pnas.0610410104. PubMed DOI PMC

Schuster A., Skinner M.K., Yan W. Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ. Epigenetics. 2016;2:dvw001. doi: 10.1093/eep/dvw001. PubMed DOI PMC

Iqbal K., Tran D.A., Li A.X., Warden C., Bai A.Y., Singh P., Wu X., Pfeifer G.P., Szabó P.E. Deleterious effects of endocrine disruptors are corrected in the mammalian germline by epigenome reprogramming. Genome Biol. 2015;16:59. doi: 10.1186/s13059-015-0619-z. PubMed DOI PMC

Salian S., Doshi T., Vanage G. Perinatal exposure of rats to Bisphenol A affects the fertility of male offspring. Life Sci. 2009;85:742–752. doi: 10.1016/j.lfs.2009.10.004. PubMed DOI

Bruner-Tran K.L., Osteen K.G. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod. Toxicol. 2011;31:344–350. doi: 10.1016/j.reprotox.2010.10.003. PubMed DOI PMC

Nilsson E., Larsen G., Manikkam M., Guerrero-Bosagna C., Savenkova M.I., Skinner M.K. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE. 2012;7:e36129. doi: 10.1371/journal.pone.0036129. PubMed DOI PMC

Mbiydzenyuy N.E., Hemmings S.M.J., Qulu L. Prenatal maternal stress and offspring aggressive behavior: Intergenerational and transgenerational inheritance. Front. Behav. Neurosci. 2022;16:977416. doi: 10.3389/fnbeh.2022.977416. PubMed DOI PMC

Fitz-James M.H., Cavalli G. Molecular mechanisms of transgenerational epigenetic inheritance. Nat. Rev. Genet. 2022;23:325–341. doi: 10.1038/s41576-021-00438-5. PubMed DOI

Sun Q., Huang S., Wang X., Zhu Y., Chen Z., Chen D. N6-methyladenine functions as a potential epigenetic mark in eukaryotes. Bioessays. 2015;37:1155–1162. doi: 10.1002/bies.201500076. PubMed DOI

Klungland A., Robertson A.B. Oxidized C5-methyl cytosine bases in DNA: 5-Hydroxymethylcytosine; 5-formylcytosine; and 5-carboxycytosine. Free. Radic. Biol. Med. 2017;107:62–68. doi: 10.1016/j.freeradbiomed.2016.11.038. PubMed DOI

Barlow D.P., Stöger R., Herrmann B.G., Saito K., Schweifer N. The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature. 1991;354:56–58. doi: 10.1038/349084a0. PubMed DOI

Santini L., Halbritter F., Titz-Teixeira F., Suzuki T., Asami M., Ma X., Ramesmayer J., Lackner A., Warr N., Pauler F., et al. Genomic imprinting in mouse blastocysts is predominantly associated with H3K27me3. Nat. Commun. 2021;12:3804. doi: 10.1038/s41467-021-23510-4. PubMed DOI PMC

Butler M.G. Imprinting disorders in humans: A review. Curr. Opin. Pediatr. 2020;32:719–729. doi: 10.1097/MOP.0000000000000965. PubMed DOI PMC

Reik W., Dean W., Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293:1089–1093. doi: 10.1126/science.1063443. PubMed DOI

Wasson J.A., Ruppersburg C.C., Katz D.J. Restoring totipotency through epigenetic reprogramming. Brief. Funct. Genom. 2013;12:118–128. doi: 10.1093/bfgp/els042. PubMed DOI PMC

Tucci V., Isles A., Kelsey G., Ferguson-Smith A.C., the Erice Imprinting Group Genomic Imprinting and Physiological Processes in Mammals. Cell. 2019;176:952–965. doi: 10.1016/j.cell.2019.01.043. PubMed DOI

Lane N., Dean W., Erhardt S., Hajkova P., Surani A., Reik W. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis. 2003;35:88–93. doi: 10.1002/gene.10168. PubMed DOI

Hackett J.A., Sengupta R., Zylicz J.J., Murakami K., Lee C., Down T.A., Surani M.A. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science. 2013;339:448–452. doi: 10.1126/science.1229277. PubMed DOI PMC

Seisenberger S., Andrews S., Krueger F., Arand J., Walter J., Santos F., Popp C., Thienpont B., Dean W., Reik W. The Dynamics of Genome-wide DNA Methylation Reprogramming in Mouse Primordial Germ Cells. Mol. Cell. 2012;48:849–862. doi: 10.1016/j.molcel.2012.11.001. PubMed DOI PMC

Kremsky I., Corces V.G. Protection from DNA re-methylation by transcription factors in primordial germ cells and pre-implantation embryos can explain trans-generational epigenetic inheritance. Genome Biol. 2020;21:118. doi: 10.1186/s13059-020-02036-w. PubMed DOI PMC

Nakamura T., Liu Y.-J., Nakashima H., Umehara H., Inoue K., Matoba S., Tachibana M., Ogura A., Shinkai Y., Nakano T. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature. 2012;486:415–419. doi: 10.1038/nature11093. PubMed DOI

Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705. doi: 10.1016/j.cell.2007.02.005. PubMed DOI

Zhu D., Zhang Y., Wang S. Histone citrullination: A new target for tumors. Mol. Cancer. 2021;20:90. doi: 10.1186/s12943-021-01373-z. PubMed DOI PMC

Shi H., Wei J., He C. Where, When, and How: Context-Dependent Functions of RNA Methylation Writers, Readers, and Erasers. Mol. Cell. 2019;74:640–650. doi: 10.1016/j.molcel.2019.04.025. PubMed DOI PMC

Gaydos L.J., Wang W., Strome S. H3K27me and PRC2 transmit a memory of repression across generations and during development. Science. 2014;345:1515–1518. doi: 10.1126/science.1255023. PubMed DOI PMC

Hammoud S.S., Nix D.A., Zhang H., Purwar J., Carrell D.T., Cairns B.R. Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009;460:473–478. doi: 10.1038/nature08162. PubMed DOI PMC

Brunner A.M., Nanni P., Mansuy I.M. Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin. 2014;7:2. doi: 10.1186/1756-8935-7-2. PubMed DOI PMC

Long J., Walker J., She W., Aldridge B., Gao H., Deans S., Vickers M., Feng X. Nurse cell –derived small RNAs define paternal epigenetic inheritance in Arabidopsis. Science. 2021;373:eabh0556. doi: 10.1126/science.abh0556. PubMed DOI

Peng H., Shi J., Zhang Y., Zhang H., Liao S., Li W., Lei L., Han C., Ning L., Cao Y., et al. A novel class of tRNA-derived small RNAs extremely enriched in mature mouse sperm. Cell Res. 2012;22:1609–1612. doi: 10.1038/cr.2012.141. PubMed DOI PMC

Bohacek J., Rassoulzadegan M. Sperm RNA: Quo vadis? Semin. Cell Dev. Biol. 2020;97:123–130. doi: 10.1016/j.semcdb.2019.07.005. PubMed DOI

Sharma U., Conine C.C., Shea J.M., Boskovic A., Derr A.G., Bing X.Y., Belleannee C., Kucukural A., Serra R.W., Sun F., et al. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science. 2015;6780:1–9. doi: 10.1126/science.aad6780. PubMed DOI PMC

Rassoulzadegan M., Grandjean V., Gounon P., Vincent S., Gillot I., Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature. 2006;441:469–474. doi: 10.1038/nature04674. PubMed DOI

Grandjean V., Fourré S., De Abreu D.A.F., Derieppe M.-A., Remy J.-J., Rassoulzadegan M. RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci. Rep. 2015;5:18193. doi: 10.1038/srep18193. PubMed DOI PMC

Chen Q., Yan M., Cao Z., Li X., Zhang Y., Shi J., Feng G.-H., Peng H., Zhang X., Zhang Y., et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2016;351:397–400. doi: 10.1126/science.aad7977. PubMed DOI

Sarker G., Sun W., Rosenkranz D., Pelczar P., Opitz L., Efthymiou V., Wolfrum C., Peleg-Raibstein D. Maternal overnutrition programs hedonic and metabolic phenotypes across generations through sperm tsRNAs. Proc. Natl. Acad. Sci. USA. 2019;116:10547–10556. doi: 10.1073/pnas.1820810116. PubMed DOI PMC

Zhang Y., Shi J., Rassoulzadegan M., Tuorto F., Chen Q. Sperm RNA code programmes the metabolic health of offspring. Nat. Rev. Endocrinol. 2019;15:489–498. doi: 10.1038/s41574-019-0226-2. PubMed DOI PMC

Gapp K., Bohacek J. Epigenetic germline inheritance in mammals: Looking to the past to understand the future. Genes Brain Behav. 2017;17:e12407. doi: 10.1111/gbb.12407. PubMed DOI

Cossetti C., Lugini L., Astrologo L., Saggio I., Fais S., Spadafora C. Soma-to-germline transmission of RNA in mice xenografted with human tumour cells: Possible transport by exosomes. PLoS ONE. 2014;9:e101629. doi: 10.1371/journal.pone.0101629. PubMed DOI PMC

Sharma U., Sun F., Conine C.C., Reichholf B., Kukreja S., Herzog V.A., Ameres S.L., Rando O.J. Small RNAs Are Trafficked from the Epididymis to Developing Mammalian Sperm. Dev. Cell. 2018;46:481–494.e6. doi: 10.1016/j.devcel.2018.06.023. PubMed DOI PMC

Sharma A. Transgenerational epigenetic inheritance: Focus on soma to germline information transfer. Prog. Biophys. Mol. Biol. 2013;113:439–446. doi: 10.1016/j.pbiomolbio.2012.12.003. PubMed DOI

Chan J.C., Nugent B.M., Morrison K.E., Jašarević E., Bhanu N.V., Garcia B.A., Bale T.L. Epididymal glucocorticoid receptors promote intergenerational transmission of paternal stress. bioRxiv. 2018. preprint . DOI

Shorter J., Lindquist S. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 2005;6:435–450. doi: 10.1038/nrg1616. PubMed DOI

Bonasio R., Tu S., Reinberg D. Molecular signals of epigenetic states. Science. 2010;330:612–616. doi: 10.1126/science.1191078. PubMed DOI PMC

Jablonka E., Raz G. Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 2009;84:131–176. doi: 10.1086/598822. PubMed DOI

Bohacek J., Mansuy J.B.I.M. A guide to designing germline-dependent epigenetic inheritance experiments in mammals. Nat. Methods. 2017;14:243–249. doi: 10.1038/nmeth.4181. PubMed DOI

Jablonka E. Epigenetic inheritance and plasticity: The responsive germline. Prog. Biophys. Mol. Biol. 2013;111:99–107. doi: 10.1016/j.pbiomolbio.2012.08.014. PubMed DOI

Komada M., Takao K., Miyakawa T. Elevated Plus Maze for Mice. J. Vis. Exp. 2008;22:1088. doi: 10.3791/1088. PubMed DOI PMC

Can A., Dao D.T., Arad M., Terrillion C.E., Piantadosi S.C., Gould T.D. The mouse forced swim test. J. Vis. Exp. 2012;59:3638. doi: 10.3791/3638. PubMed DOI PMC

Francis D.D., Meaney M.J. Maternal care and the development of stress responses. Curr. Opin. Neurobiol. 1999;9:128–134. doi: 10.1016/S0959-4388(99)80016-6. PubMed DOI

Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol. Behav. 2003;79:359–371. doi: 10.1016/S0031-9384(03)00149-5. PubMed DOI

Weaver I.C., Cervoni N., Champagne F.A., D’Alessio A.C., Sharma S., Seckl J.R., Dymov S., Szyf M., Meaney M.J. Epi-genetic programming by maternal behavior. Nat. Neurosci. 2004;7:847–854. doi: 10.1038/nn1276. PubMed DOI

Timmermans S., Souffriau J., Libert C. A general introduction to glucocorticoid biology. Front. Immunol. 2019;10:1545. doi: 10.3389/fimmu.2019.01545. PubMed DOI PMC

Babb J.A., Carini L.M., Spears S.L., Nephew B.C. Transgenerational effects of social stress on social behavior, corticosterone, oxytocin, and prolactin in rats. Horm. Behav. 2014;65:386–393. doi: 10.1016/j.yhbeh.2014.03.005. PubMed DOI PMC

McGowan P.O., Sasaki A., D’Alessio A.C., Dymov S., Labonté B., Szyf M., Turecki G., Meaney M.J. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 2009;12:342–348. doi: 10.1038/nn.2270. PubMed DOI PMC

McCreary J.K., Truica L.S., Friesen B., Yao Y., Olson D.M., Kovalchuk I., Cross A.R., Metz G.A. Altered brain morphology and functional connectivity reflect a vulnerable affective state after cumulative multigenerational stress in rats. Neuroscience. 2016;330:79–89. doi: 10.1016/j.neuroscience.2016.05.046. PubMed DOI

Bohacek J., Farinelli M., Mirante O., Steiner G., Gapp K., Coiret G., Ebeling M., Durán-Pacheco G., Iniguez A.L., Manuella F., et al. Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress. Mol. Psychiatry. 2015;20:621–631. doi: 10.1038/mp.2014.80. PubMed DOI

Labonte B., Yerko V., Gross J., Mechawar N., Meaney M.J., Szyf M., Turecki G. Differential glucocorticoid receptor exon 1 B, 1 C, and 1 H expression and methylation in suicide completers with a history of childhood abuse. Biol. Psychiatry. 2012;72:41–48. doi: 10.1016/j.biopsych.2012.01.034. PubMed DOI

De Bellis M.D., Chrousos G.P., Dorn L.D., Burke L., Helmers K., Kling M.A., Trickett P.K., Putnam F.W. Hypothalamic-Pituitary-Adrenal Axis Dysregulation in Sexually abused Girls. J. Clin. Endocrinol. Metab. 1994;78:249–255. PubMed

Vythilingam M., Heim C., Newport D.J., Miller A.H., Anderson E., Bronen R., Brummer M., Staib L., Vermetten E., Charney D.S., et al. Childhood Trauma Associated With Smaller Hippocampal Volume in Women With Major Depression. Am. J. Psychiatry. 2002;159:2072–2080. doi: 10.1176/appi.ajp.159.12.2072. PubMed DOI PMC

Oberlander T.F., Weinberg J., Papsdorf M., Grunau R., Misri S., Devlin A.M. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008;3:97–106. doi: 10.4161/epi.3.2.6034. PubMed DOI

Aoued H.S., Sannigrahi S., Hunter S.C., Doshi N., Sathi Z.S., Chan A.W.S., Walum H., Dias B.G. Proximate causes and consequences of intergenerational influences of salient sensory experience. Genes Brain Behav. 2020;19:e12638. doi: 10.1111/gbb.12638. PubMed DOI PMC

Gapp K., van Steenwyk G., Germain P.L., Matsushima W., Rudolph K.L.M., Manuella F., Roszkowski M., Vernaz G., Ghosh T., Pelczar P., et al. Alterations in sperm long RNA contribute to the epigenetic inheritance of the effects of postnatal trauma. Mol. Psychiatry. 2020;25:2162–2174. doi: 10.1038/s41380-018-0271-6. PubMed DOI PMC

Roseboom T.J., van der Meulen J.H.P., Osmond C., Barker D.J.P., Ravelli A.C.J., Schroeder-Tanka J.M., van Montfrans G.A., Michels R.P.J., Bleker O.P. Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart. 2000;84:595–598. doi: 10.1136/heart.84.6.595. PubMed DOI PMC

Painter R.C., De Rooij S.R., Bossuyt P.M., Simmers T.A., Osmond C., Barker D.J., Bleker O.P., Roseboom T.J. Early onset of coronary artery disease after prenatal exposure to the Dutch famine1–3. Am. J. Clin. Nutr. 2006;84:322–327. doi: 10.1093/ajcn/84.2.322. PubMed DOI

Hoek H.W., Susser E., Buck K.A., Lumey L.H., Lin S.P., Gorman J.M. Schizoid Personality Disorder After Prenatal Exposure to Famine. Am. J. Psychiatry. 1996;153:1637–1639. PubMed

Painter R., Osmond C., Gluckman P., Hanson M., Phillips D., Roseboom T. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG Int. J. Obstet. Gynaecol. 2008;115:1243–1249. doi: 10.1111/j.1471-0528.2008.01822.x. PubMed DOI

Veenendaal M.V., Painter R.C., de Rooij S.R., Bossuyt P.M., van der Post J.A., Gluckman P.D., Hanson M.A., Roseboom T.J. Transgenerational effects of prenatal exposure to the 1944–45 Dutch famine. BJOG Int. J. Obstet. Gynaecol. 2013;120:548–554. doi: 10.1111/1471-0528.12136. PubMed DOI

Rotar O., Moguchaia E., Boyarinova M., Kolesova E., Khromova N., Freylikhman O., Smolina N., Solntsev V., Kostareva A., Konradi A., et al. Seventy years after the siege of Leningrad: Does early life famine still affect cardiovascular risk and aging? J. Hypertens. 2015;33:1772–1779. doi: 10.1097/HJH.0000000000000640. PubMed DOI

Lumey L., Stein A.D., Susser E. Prenatal famine and adult health. Annu. Rev. Public Health. 2011;32:237–262. doi: 10.1146/annurev-publhealth-031210-101230. PubMed DOI PMC

van den Berg G.J., Pinger P.R. Transgenerational effects of childhood conditions on third generation health and education outcomes. Econ. Hum. Biol. 2016;23:103–120. doi: 10.1016/j.ehb.2016.07.001. PubMed DOI

Lehrner A., Yehuda R. Trauma across generations and paths to adaptation and resilience. Psychol. Trauma Theory Res. Pract. Policy. 2018;10:22–29. doi: 10.1037/tra0000302. PubMed DOI

Yehuda R., Schmeidler J., Wainberg M., Binder-Brynes K., Duvdevani T. Vulnerability to posttraumatic stress disorder in adult offspring of Holocaust survivors. Am. J. Psychiatry. 1998;155:1163–1171. doi: 10.1176/ajp.155.9.1163. PubMed DOI

Yehuda R., Koenen K.C., Galea S., Flory J.D. The role of genes in defining a molecular biology of PTSD. Dis. Markers. 2011;30:67–76. doi: 10.1155/2011/185354. PubMed DOI PMC

Lehrner A., Bierer L.M., Passarelli V., Pratchett L.C., Flory J.D., Bader H.N., Harris I.R., Bedi A., Daskalakis N.P., Makotkine I., et al. Maternal PTSD associates with greater glucocorticoid sensitivity in offspring of Holocaust survivors. Psychoneuroendocrinology. 2014;40:213–220. doi: 10.1016/j.psyneuen.2013.11.019. PubMed DOI PMC

Kertes D.A., Kamin H.S., Hughes D.A., Rodney N.C., Bhatt S., Mulligan C.J. Prenatal Maternal Stress Predicts Methylation of Genes Regulating the Hypothalamic–Pituitary–Adrenocortical System in Mothers and Newborns in the Democratic Republic of Congo. Child Dev. 2016;87:61–72. doi: 10.1111/cdev.12487. PubMed DOI PMC

Yehuda R., Daskalakis N.P., Bierer L.M., Bader H.N., Klengel T., Holsboer F., Binder E.B. Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation. Biol. Psychiatry. 2016;80:372–380. doi: 10.1016/j.biopsych.2015.08.005. PubMed DOI

Rowland-Klein D., Dunlop R. Handbook of Stress, Trauma, and the Family. Routledge/Taylor & Francis Group; London, UK: 2013. The Transmission of Trauma across Generations: Identification with Parental Trauma in Children of Holocaust Survivors; pp. 117–136. PubMed

Van Ijzendoorn M.H., Bakermans-Kranenburg M.J., Sagi-Schwartz A. Are Children of Holocaust Survivors Less Well-Adapted? A Meta-Analytic Investigation of Secondary Traumatization. J. Trauma. Stress. 2003;16:459–469. doi: 10.1023/A:1025706427300. PubMed DOI

Gapp K., Soldado-Magraner S., Alvarez-Sánchez M., Bohacek J., Vernaz G., Shu H., Franklin T., Wolfer D.P., Mansuy I.M. Early life stress in fathers improves behavioural flexibility in their offspring. Nat. Commun. 2014;5:5466. doi: 10.1038/ncomms6466. PubMed DOI

Levav I., Levinson D., Radomislensky I., Shemesh A.A., Kohn R. Psychopathology and other health dimensions among the offspring of Holocaust survivors: Results from the Israel National Health Survey. Isr. J. Psychiatry Relat. Sci. 2007;44:144–151. PubMed

Sagi-Schwartz A., Van Ijzendoorn M.H., Bakermans-Kranenburg M.J. Does intergenerational transmission of trauma skip a generation? No meta-analytic evidence for tertiary traumatization with third generation of Holocaust survivors. Attach. Hum. Dev. 2008;10:105–121. doi: 10.1080/14616730802113661. PubMed DOI

Dias B.G., Ressler K. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 2014;17:89–96. doi: 10.1038/nn.3594. PubMed DOI PMC

Morrison F.G., Dias B.G., Ressler K.J. Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size. Proc. Natl. Acad. Sci. USA. 2015;112:12846–12851. doi: 10.1073/pnas.1505068112. PubMed DOI PMC

Aoued H.S., Sannigrahi S., Doshi N., Morrison F.G., Linsenbaum H., Hunter S.C., Walum H., Baman J., Yao B., Jin P., et al. Reversing Behavioral, Neuroanatomical, and Germline Influences of Intergenerational Stress. Biol. Psychiatry. 2019;85:248–256. doi: 10.1016/j.biopsych.2018.07.028. PubMed DOI PMC

Benito E., Kerimoglu C., Ramachandran B., Pena-Centeno T., Jain G., Stilling R.M., Islam R., Capece V., Zhou Q., Edbauer D., et al. RNA-Dependent Intergenerational Inheritance of Enhanced Synaptic Plasticity after Environmental Enrichment. Cell Rep. 2018;23:546–554. doi: 10.1016/j.celrep.2018.03.059. PubMed DOI PMC

Gapp K., Jawaid A., Sarkies P., Bohacek J., Pelczar P., Prados J., Farinelli L., Miska E., Mansuy I.M. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 2014;17:667–669. doi: 10.1038/nn.3695. PubMed DOI PMC

Rodgers A.B., Morgan C.P., Leu N.A., Bale T.L. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl. Acad. Sci. USA. 2015;112:13699–13704. doi: 10.1073/pnas.1508347112. PubMed DOI PMC

Jawaid A., Kunzi M., Mansoor M., Khan Z.Y., Abid A., Taha M., Rigotti S., Thumfart K., Faisal S., Chughtai O., et al. Distinct microRNA signature in human serum and germline after childhood trauma. medRxiv. 2020. preprint . DOI

Van Steenwyk G., Roszkowski M., Manuella F., Franklin T.B., Mansuy I.M. Transgenerational inheritance of behavioral and metabolic effects of paternal exposure to traumatic stress in early postnatal life: Evidence in the 4th generation. Environ. Epigenetics. 2018;4:dvy023. doi: 10.1093/eep/dvy023. PubMed DOI PMC

Ptashne M. Epigenetics: Core misconcept. Proc. Natl. Acad. Sci. USA. 2013;110:7101–7103. doi: 10.1073/pnas.1305399110. PubMed DOI PMC

Heard E., Martienssen R.A. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell. 2014;157:95–109. doi: 10.1016/j.cell.2014.02.045. PubMed DOI PMC

Horsthemke B. A critical view on transgenerational epigenetic inheritance in humans. Nat. Commun. 2018;9:2973. doi: 10.1038/s41467-018-05445-5. PubMed DOI PMC

Grossniklaus U., Kelly W., Ferguson-Smith A., Pembrey M., Lindquist S. Transgenerational epigenetic inheritance: How important is it? [(accessed on 10 November 2022)];Nat. Rev. Genet. 2013 14:228–235. doi: 10.1038/nrg3435. Available online: www.nature.com/reviews/genetics%0Ahttp://lindquistlab.wi.mit.edu/wp-content/uploads/2013/06/Grossniklaus2013NatRevGenet.pdf. PubMed DOI PMC

van Otterdijk S.D., Michels K.B. Transgenerational epigenetic inheritance in mammals: How good is the evidence? FASEB J. 2016;30:2457–2465. doi: 10.1096/fj.201500083. PubMed DOI

Kaiser J. The Epigenetics Heretic. Science. 2014;343:361–363. doi: 10.1126/science.343.6169.361. PubMed DOI

Guéant J.-L., Chéry C., Oussalah A., Nadaf J., Coelho D., Josse T., Flayac J., Robert A., Koscinski I., Gastin I., et al. APRDX1 mutant allele causes a MMACHC secondary epimutation in cblC patients. Nat. Commun. 2018;9:67. doi: 10.1038/s41467-017-02306-5. PubMed DOI PMC

Tufarelli C., Sloane-Stanley J.A., Garrick D., Sharpe J.A., Ayyub H., Wood W.G., Higgs D.R. Transcription of antisense RNA leading to gene silencing and methylation as a novel cause of human genetic disease. Nat. Genet. 2003;34:157–165. doi: 10.1038/ng1157. PubMed DOI

Mitchell K. Calibrating Scientific Skepticism—A Wider Look at the Field of Transgenerational Epigenetics. 2018. Blog Entry. [(accessed on 10 November 2022)]. Available online: http://www.wiringthebrain.com/2018/07/calibrating-scientific-skepticism-wider.html.

Uller T., English S., Pen I. When is incomplete epigenetic resetting in germ cells favoured by natural selection? Proc. R. Soc. B Boil. Sci. 2015;282:20150682. doi: 10.1098/rspb.2015.0682. PubMed DOI PMC

Lachmann M., Jablonka E. The inheritance of phenotypes: An adaptation to fluctuating environments. J. Theor. Biol. 1996;181:1–9. doi: 10.1006/jtbi.1996.0109. PubMed DOI

Fullston T., Teague E.M.C.O., Palmer N.O., DeBlasio M.J., Mitchell M., Corbett M., Print C.G., Owens J.A., Lane M. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013;27:4226–4243. doi: 10.1096/fj.12-224048. PubMed DOI

Fullston T., Ohlsson-Teague E.M.C., Print C.G., Sandeman L.Y., Lane M. Sperm microRNA content is altered in a mouse model of male obesity, but the same suite of microRNAs are not altered in offspring’s sperm. PLoS ONE. 2016;11:e0166076. doi: 10.1371/journal.pone.0166076. PubMed DOI PMC

Portin P. Does epigenetic inheritance revolutionize the foundations of the theory of evolution? [(accessed on 14 November 2022)];Curr. Top. Genet. 2012 5 Available online: http://www.researchtrends.net/tia/article_pdf.asp?in=0&vn=5&tid=45&aid=3652.

Laland K.N., Uller T., Feldman M.W., Sterelny K., Müller G.B., Moczek A.P., Jablonka E., Odling-Smee F.J. The extended evolutionary synthesis: Its structure, assumptions and predictions. Proc. R. Soc. B Boil. Sci. 2015;282:20151019. doi: 10.1098/rspb.2015.1019. PubMed DOI PMC

West-Eberhard M.J. Developmental Plasticity and Evolution. Oxford University Press; Oxford, UK: 2003.

Baldwin J.M. A New Factor in Evolution Published by: The University of Chicago Press for the American Society of Naturalists Stable. [(accessed on 10 November 2022)];Am. Nat. 1896 30:441–451. doi: 10.1086/276408. Available online: http://www.jstor.org/stable/2453130. DOI

Waddington C. Genetic Assimilation of an Acquired Character. Evolution. 1952;7:118–126.

Waddington C.H. Genetic Assimilation of the Bithorax Phenotype. Evolution. 1956;10:1–13. doi: 10.2307/2406091. DOI

Turner B.M. Epigenetic responses to environmental change and their evolutionary implications. Philos. Trans. R. Soc. B Biol. Sci. 2009;364:3403–3418. doi: 10.1098/rstb.2009.0125. PubMed DOI PMC

Hernando-Herraez I., Heyn H., Fernandez-Callejo M., Vidal E., Bellon H.F., Prado-Martinez J., Sharp A.J., Esteller M., Marques-Bonet T. The interplay between DNA methylation and sequence divergence in recent human evolution. Nucleic Acids Res. 2015;43:8204–8214. doi: 10.1093/nar/gkv693. PubMed DOI PMC

Makova K.D., Hardison R. The effects of chromatin organization on variation in mutation rates in the genome. Nat. Rev. Genet. 2015;16:213–223. doi: 10.1038/nrg3890. PubMed DOI PMC

Stotz K. Extended evolutionary psychology: The importance of transgenerational developmental plasticity. Front. Psychol. 2014;5:908. doi: 10.3389/fpsyg.2014.00908. PubMed DOI PMC

Robinson G.E., Barron A.B. Epigenetics and the evolution of instincts: Instincts may evolve from learning and share the same cellular and molecular mechanisms. Science. 2017;356:26–27. doi: 10.1126/science.aam6142. PubMed DOI

Weiner A.K.M., Katz L.A. Epigenetics as Driver of Adaptation and Diversification in Microbial Eukaryotes. Front. Genet. 2021;12:642220. doi: 10.3389/fgene.2021.642220. PubMed DOI PMC

Thorson J.L., Smithson M., Beck D., Sadler-Riggleman I., Nilsson E., Dybdahl M., Skinner M.K. Epigenetics and adaptive phenotypic variation between habitats in an asexual snail. Sci. Rep. 2017;7:14139. doi: 10.1038/s41598-017-14673-6. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...