Skip to main content

Epigenetic Inheritance in Mammals

  • Chapter
  • First Online:
Epigenetics, Brain and Behavior

Part of the book series: Research and Perspectives in Neurosciences ((NEUROSCIENCE))

Abstract

The epigenetic state of a cell is determined by epigenome that represents the ensemble of modifications occurring at the chromatin. These modifications involve the specific marking of DNA and protein histones, which provides a potent and dynamic mode of regulation of the genome without changing the DNA sequence itself. In mammals, the epigenome was previously thought to be fully erased after fertilization and then partly reestablished for further cellular development and differentiation. It is now recognized that erasure is not complete and that some epigenetic marks are maintained and passed to the offspring. Such maintenance is postulated to provide a unique mode of epigenetic inheritance, but this proposal has been the subject of much debate. Now, there is increasing evidence to show that it does occur in rodents and humans. This review discusses some of this evidence and describes examples of epigenomic transmission of traits influenced by environmental factors such as diet, toxic agents, stress and environmental enrichment across generations.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469

    Article  PubMed  CAS  Google Scholar 

  • Arai JA, Li S, Hartley DM, Feig LA (2009) Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment. J Neurosci 29:1496–1502

    Article  PubMed  CAS  Google Scholar 

  • Arnaud P (2010) Genomic imprinting in germ cells: imprints are under control. Reproduction 140:411–423

    Article  PubMed  CAS  Google Scholar 

  • Benyshek DC, Johnston CS, Martin JF (2006) Glucose metabolism is altered in the adequately-nourished grand-offspring (F3 generation) of rats malnourished during gestation and perinatal life. Diabetologia 49:1117–1119

    Article  PubMed  CAS  Google Scholar 

  • Blatt J, Van Le L, Weiner T, Sailer S (2003) Ovarian carcinoma in an adolescent with transgenerational exposure to diethylstilbestrol. J Pediatr Hematol Oncol 25:635–636

    Article  PubMed  Google Scholar 

  • Bromer JG, Wu J, Zhou Y, Taylor HS (2009) Hypermethylation of homeoboxA10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 150:3376–3382

    Article  PubMed  CAS  Google Scholar 

  • Bygren L, Kaati G, Edvinsson S (2001) Longevity determined by paternal ancestors’ nutrition during their slow growth period. Acta Biotheor 49:53–59

    Article  PubMed  CAS  Google Scholar 

  • Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, GuH ZPD, Meissner A, Weng Z, Hofmann HA, Friedman N, Rando OJ (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084–1096

    Article  PubMed  CAS  Google Scholar 

  • Curley JP, Jensen CL, Mashoodh R, Champagne FA (2011a) Socialinfluences on neurobiology and behavior: epigenetic effects during development. Psychoneuroendocrinology 36:352–371

    Article  PubMed  CAS  Google Scholar 

  • Curley JP, Mashoodh R, Champagne FA (2011b) Epigenetics and the origins of paternal effects. Horm Behav 59:306–314

    Article  PubMed  Google Scholar 

  • Daxinger L, Whitelaw E (2010) Transgenerational epigenetic inheritance: more questions than answers. Genome Res 20:1623–1628

    Article  PubMed  CAS  Google Scholar 

  • Dierker LC, Merikangas KR, Szatmari P (1999) Influence of parental concordance for psychiatric disorders on psychopathology in offspring. J Am Acad Child Adolesc Psychiatry 38:280–288

    Article  PubMed  CAS  Google Scholar 

  • Dunn GA, Bale TL (2009) Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150:4999–5009

    Article  PubMed  CAS  Google Scholar 

  • Eun SH, Gan Q, Chen X (2010) Epigenetic regulation of germ cell differentiation. Curr Opin Cell Biol 22:737–743

    Article  PubMed  CAS  Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  PubMed  CAS  Google Scholar 

  • Franklin TB, Mansuy IM (2010a) Epigenetic inheritance in mammals: evidence for the impact of adverse environmental effects. Neurobiol Dis 39:61–65

    Article  PubMed  CAS  Google Scholar 

  • Franklin TB, Mansuy IM (2010b) The prevalence of epigenetic mechanisms in the regulation of cognitive functions and behaviour. Curr Opin Neurobiol 20:441–449

    Article  PubMed  CAS  Google Scholar 

  • Franklin TB, Russig H, Weiss IC, Gräff J, Linder N, Michalon A, Vizi S, Mansuy IM (2010) Epigenetic transmission of the impact of early stress across generations. Biol Psychiatry 68:408–415

    Article  PubMed  Google Scholar 

  • Godfrey KM, Gluckman PD, Hanson MA (2010) Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab 21:199–205

    Article  PubMed  CAS  Google Scholar 

  • Guerrero-Bosagna C, Settles M, Lucker B, Skinner MK (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS One 5:e13100

    Article  PubMed  Google Scholar 

  • Harper LV (2005) Epigenetic inheritance and the intergenerational transfer of experience. Psychol Bull 131:340–360

    Article  PubMed  Google Scholar 

  • Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, LeBouc Y, Deal CL, Lillycrop K, Scharfmann R, Sheppard A, Skinner M, Szyf M, Waterland RA, Waxman DJ, Whitelaw E, Ong K, Albertsson-Wikland K (2011) Child health, developmental plasticity, and epigenetic programming. Endocr Rev 32:159–224

    Article  PubMed  CAS  Google Scholar 

  • Iversen AC, Fear NT, Simonoff E, Hull L, Horn O, Greenberg N, Hotopf M, Rona R, Wessely S (2007) Influence of childhood adversity on health among male UK military personnel. Br J Psychiatry 191:506–511

    Article  PubMed  Google Scholar 

  • Jirtle RL, Skinner MK (2007) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253–262

    Article  PubMed  CAS  Google Scholar 

  • Kaati G, Bygren LO, Pembrey M, Sjostrom M (2007) Transgenerational response to nutrition, early life circumstances and longevity. Eur J Hum Genet 15:784–790

    Article  PubMed  CAS  Google Scholar 

  • Li S, Hansman R, Newbold R, Davis B, McLachlan JA, Barrett JC (2003) Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol Carcinog 38:78–84

    Article  PubMed  CAS  Google Scholar 

  • Manassis K, Bradley S, Goldberg S, Hood J, Swinson RP (1995) Behavioural inhibition, attachment and anxiety in children of mothers with anxiety disorders. Can J Psychiatry 40:87–92

    PubMed  CAS  Google Scholar 

  • McGowan PO, Sasaki A, Huang TC, Unterberger A, Suderman M, Ernst C, Meaney MJ, Turecki G, Szyf M (2008) Promoter-wide hypermethylation of the ribosomal RNA gene promoter in the suicide brain. PLoS One 3:e2085

    Article  PubMed  Google Scholar 

  • McKay JA, Mathers JC (2011) Diet induced epigenetic changes and their implications for health. Acta Physiol 202:103–118

    Article  CAS  Google Scholar 

  • Merikangas KR, Swendsen JD, Preisig MA, Chazan RZ (1998) Psychopathology and temperament in parents and offspring: results of a family study. J Affect Disord 51:63–74

    Article  PubMed  CAS  Google Scholar 

  • Newbold RR, Padilla-Banks E, Jefferson WN (2006) Adverse effects of themodel environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147:S11–S17

    Article  PubMed  CAS  Google Scholar 

  • Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467:963–966

    Article  PubMed  CAS  Google Scholar 

  • Palmer JR, Wise LA, Hatch EE, Troisi R, Titus-Ernstoff L, Strohsnitter W, Kaufman R, Herbst AL, Noller KL, Hyer M, Hoover RN (2006) Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomarkers Prev 15:1509–1514

    Article  PubMed  CAS  Google Scholar 

  • Pembrey ME (2010) Male-line transgenerational responses in humans. Hum Fertil (Camb) 13:268–271

    Article  Google Scholar 

  • Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159–166

    Article  PubMed  Google Scholar 

  • Shamir-Essakow G, Ungerer JA, Rapee RM (2005) Attachment, behavioural inhibition, and anxiety in preschool children. J Abnorm Child Psychol 33:131–143

    Article  PubMed  Google Scholar 

  • Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21:214–222

    Article  PubMed  CAS  Google Scholar 

  • Sroufe LA (2002) From infant attachment to promotion of adolescent autonomy: prospective, longitudinal data on the role of parents. In: Borkowski JG, Bristol-Power M (eds) Parenting and the child’s world: influences on academic, intellectual and socio-emotional development. Erlbaum, Mahwah, pp 187–202

    Google Scholar 

  • Stouder C, Paoloni-Giacobino A (2010) Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 139:373–379

    Article  PubMed  CAS  Google Scholar 

  • Susser M, Stein Z (1994) Timing in prenatal nutrition: a reprise of the Dutch famine study. Nutr Rev 52:84–94

    Article  PubMed  CAS  Google Scholar 

  • Titus-Ernstoff L, Troisi R, Hatch EE, Hyer M, Wise LA, Palmer JR, KaufmanR AE, Noller K, Herbst AL, Strohsnitter W, Cole BF, Hartge P, Hoover RN (2008) Offspring of women exposed in utero to diethylstilbestrol (DES): a preliminary report of benign and malignant pathology in the third generation. Epidemiology 19:251–257

    Article  PubMed  Google Scholar 

  • Walker BE, Haven MI (1997) Intensity of multigenerational carcinogenesis from diethylstilbestrol in mice. Carcinogenesis 18:791–793

    Article  PubMed  CAS  Google Scholar 

  • Weaver IC (2007) Epigenetic programming by maternal behavior and pharmacological intervention. Epigenetics 2:22–28

    Article  PubMed  Google Scholar 

  • Weiss IC, Franklin TB, Vizi SN, Mansuy IM (2011) Inheritable effect of unpredictable maternal separation on behavioral responses in mice. Front Behav Neurosci 5:3

    Article  PubMed  Google Scholar 

  • Weissman MM, Leckman JF, Merikangas KR, Gammon GD, Prusoff BA (1984) Depression and anxiety disorders in parents and children. Results from the Yale family study. Arch Gen Psychiatry 41:845–852

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Isabelle M. Mansuy .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bohacek, J., Mansuy, I.M. (2012). Epigenetic Inheritance in Mammals. In: Sassone Corsi, P., Christen, Y. (eds) Epigenetics, Brain and Behavior. Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27913-3_5

Download citation

Publish with us

Policies and ethics