TRANSGENERATIONAL INHERITANCE OF LONGEVITY: THEORETICAL FRAMEWORK AND EMPIRICAL EVIDENCE
Abstract
A number of experimental and epidemiological investigations have provided evidence that the health status and aging rate may largely depend on the conditions in which an organism’s early development takes place. In several recent studies, data are obtained suggesting that the effects of stresses in an early development can be inherited transgenerationally, causing changes of various characteristics in subsequent generations. There have been shown that epigenetic regulation of genetic expression, including DNA methylation, histone and microRNAs modifications, can play a key role in transgenerational inheritance. Until now, it has been generally accepted that the complete erasure of epigenetic marks takes place during the gametogenesis and early embryogenesis. In recent years, however, data were provided demonstrating that epigenetic marks could be not erased completely during these periods of early ontogenesis and some of them can likely be transmitted to the descendants of several generations affecting their phenotype. In this review, the data of epidemiological and experimental studies are provided showing the possibility of inheritance of life expectancy and associated with longevity traits in several generations.
About the Authors
O. G. ZabugaUkraine
Laboratory of epigenetics
A. M. Vaiserman
Ukraine
Laboratory of epigenetics
References
1. Padmanabhan V., Cardoso R.C., Puttabyatappa M. Developmental programming, a pathway to disease // Endocrinology. 2016. Vol. 157. N 4. P. 1328–1340.
2. Bateson P., Gluckman P., Hanson M. The biology of developmental plasticity and the Predictive Adaptive Response hypothesis // J. Physiol. 2014. Vol. 592. N 11. P. 2357–2368.
3. Vaiserman A. Epidemiologic evidence for association between adverse environmental exposures in early life and epigenetic variation: a potential link to disease susceptibility? // Clin. Epigenetics. 2015. Vol. 7. N 1. P. 96.
4. Vaiserman A.M. Early-life nutritional programming of longevity // J. Dev. Orig. Health Dis. 2014. Vol. 5. N 5. 325–338.
5. Berger S.L., Kouzarides T., Shiekhattar R., Shilatifard A. An operational definition of epigenetics // Genes Dev. 2009. Vol. 23. N 7. P. 781–783.
6. van Otterdijk S.D., Michels K.B. Transgenerational epigenetic inheritance in mammals: how good is the evidence? // FASEB J. 2016. Vol. 30. N 7. P. 2457–2465.
7. Ashapkin V.V., Kutueva L.I., Vanyushin B.F. Aging epigenetics: accumulation of errors or realization of a specific program? // Biochemistry (Mosc). 2015. Vol. 80. N 11. P. 1406–1417.
8. Johnson A.A., Akman K., Calimport S.R., Wuttke D., Stolzing A., de Magalhães J.P. The role of DNA methylation in aging, rejuvenation, and age-related disease // Rejuvenation Res. 2012. Vol. 15. N 5. P. 483–494.
9. Zheng S.C., Widschwendter M., Teschendorff A.E. Epigenetic drift, epigenetic clocks and cancer risk // Epigenomics. 2016. Vol. 8. N 5. P. 705–719.
10. Blake G.E., Watson E.D. Unravelling the complex mechanisms of transgenerational epigenetic inheritance // Curr. Opin. Chem. Biol. 2016. Vol. 33. P. 101–107.
11. Rando O.J. Intergenerational transfer of epigenetic information in sperm // Cold Spring Harb. Perspect. Med. 2016. Vol. 6. N 5. a022988.
12. Hanson M.A., Low F.M., Gluckman P.D. Epigenetic epidemiology: the rebirth of soft inheritance // Ann. Nutr. Metab. 2011. Vol. 58. Suppl. 2. P. 8–15.
13. Grossniklaus U., Kelly B., Ferguson-Smith A.C., Pembrey M., Lindquist S. Transgenerational epigenetic inheritance: how important is it? // Nat. Rev. Genet. 2013. Vol. 14. N 3. P. 228–235.
14. Aiken C.E., Tarry-Adkins J.L., Ozanne S.E. Transgenerational effects of maternal diet on metabolic and reproductive ageing // Mamm. Genome. 2016. Vol. 27. N 7–8. P. 430–439.
15. Painter R.C., Osmond C., Gluckman P., Hanson M., Phillips D.I.W., Roseboom T.J. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life // BJOG. 2008. Vol. 115. N 10. P. 1243–1249.
16. Veenendaal M.V., Painter R.C., de Rooij S.R., Bos suyt 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. 2013. Vol. 120. N 5. P. 548–553.
17. Li Q., An L. Intergenerational health consequences of the 1959-1961 Great Famine on children in rural China // Econ. Hum. Biol. 2015. Vol. 18. P. 27–40.
18. Alwasel S.H., Harrath A., Aljarallah J.S., Abotalib Z., Osmond C., Al Omar S.Y. Khaled I., Barker D.J. Intergenerational effects of in utero exposure to Ramadan in Tunisia // Am. J. Hum. Biol. 2013. Vol. 25. N 3. P. 341–343.
19. Fleming J.L., Huang T.H., Toland A.E. The role of parental and grandparental epigenetic alterations in familial cancer risk // Cancer Res. 2008. Vol. 68. N 22. P. 9116–9121.
20. Bygren L.O., Kaati G., Edvinsson S. Longevity determined by paternal ancestors’ nutrition during their slow growth period // Acta Biotheor. 2001. Vol. 49. N 1. P. 53–59.
21. Kaati G., Bygren L.O., Edvinsson S. Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period // Eur. J. Hum. Genet. 2002. Vol. 10. N 11. P. 682–688.
22. Pembrey M.E.et al. Sex-specific, male-line transgenerational responses in humans // Eur. J. Hum. Genet. 2006. Vol. 14. N 2. P. 159–166.
23. Kaati G., Bygren L.O., Pembrey M., Sjöström M. Transgenerational response to nutrition, early life circumstances and longevity // Eur. J. Hum. Genet. 2007. Vol. 15. N 7. P. 784–790.
24. Pembrey M.E. Male-line transgenerational responses in humans // Hum. Fertil. (Camb.). 2010. Vol. 13. N 4. 268–271.
25. Bygren L.O., Tinghög P., Carstensen J., Edvinsson S., Kaati G., Pembrey M.E., Sjöström M. Change in paternal grandmothers’ early food supply influenced cardiovascular mortality of the female grandchildren // BMC Genet. 2014. Vol. 15. P. 12.
26. Pembrey M., Saffery R., Bygren L.O.; Network in Epigenetic Epidemiology. Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research // J. Med. Genet. 2014. Vol. 51. N 9. P. 563–572.
27. Modin B., Koupil I., Vågerö D. The impact of early twentieth century illegitimacy across three generations. Longevity and intergenerational health correlates // Soc. Sci. Med. 2009. Vol. 68. N 9. P. 1633–1640.
28. Titus-Ernstoff L., Troisi R., Hatch E.E., Hyer M., Wise L.A., Palmer J.R. Kaufman R., Adam E., Noller K., Herbst A.L., Strohsnitter W., Cole B.F., Hartge P., Hoover R.N. Offspring of women exposed in utero to diethylstilbestrol (DES): a preliminary report of benign and malignant pathology in the third generation // Epidemiology. 2008. Vol. 19. N 2. P. 251–257.
29. Northstone K., Golding J., Davey Smith G., Miller L.L., Pembrey M. Prepubertal start of father’s smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses // Eur. J. Hum. Genet. 2014. Vol. 22. N 12. P. 1382–1386.
30. Ho D.H., Burggren W.W. Epigenetics and transgenerational transfer: a physiological perspective // J. Exp. Biol. 2010. Vol. 213. N 1. P. 3–16.
31. Hackett J.A., Surani M.A. DNA methylation dynamics during the mammalian life cycle // Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2013. Vol. 368. N 1609. 20110328.
32. Jablonka E. Epigenetic inheritance and plasticity: The responsive germline // Prog. Biophys. Mol. Biol. 2013. Vol. 111. N 2–3. P. 99–107.
33. Halfmann R., Lindquist S. Epigenetics in the extreme: prions and the inheritance of environmentally acquired traits // Science. 2010. Vol. 330. N 6004. P. 629–632.
34. 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. Vol. 479. N 7373. P. 365–373.
35. Lim J.P., Brunet A. Bridging the transgenerational gap with epigenetic memory // Trends Genet. 2013. Vol. 29. N 3. P. 176–186.
36. Xia B., de Belle J.S. Transgenerational programming of longevity and reproduction by post-eclosion dietary manipulation in Drosophila // Aging (Albany NY). 2016. Vol. 8. N 5. P. 1115–1134.
37. Buescher J.L., Musselman L.P., Wilson C.A., Lang T., Keleher M., Baranski T.J., Duncan J.G. Evidence for transgenerational metabolic programming in Drosophila // Dis. Model. Mech. 2013. Vol. 6. N 5. P. 1123–1132.
38. Lombó M., Fernández-Díez C., González-Rojo S., Navarro C., Robles V., Herráez M.P. Transgenerational inheritance of heart disorders caused by paternal bisphenol A exposure // Environ. Pollut. 2015. Vol. 206. P. 667–678.
39. Avogaro A., de Kreutzenberg S.V., Fadini G.P. Insulin signaling and life span // Pflugers Arch. 2010. Vol. 459. N 2. P. 301–314.
40. Brun J.M., Bernadet M.D., Cornuez A., Leroux S., Bodin L., Basso B., Davail S., Jaglin M., Lessire M., Martin X., Sellier N., Morisson M., Pitel F. Influence of grand-mother diet on
41. offspring performances through the male line in Muscovy duck // BMC Genet. 2015. Vol. 16. P. 145. 41. Carone B.R., Fauquier L., Habib N., Shea J.M., Hart C.E., Li R., Bock C., Li C., Gu H., Zamore P.D., Meissner A., Weng Z., Hofmann H.A., Friedman N., Rando O.J. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals // Cell. 2010. Vol. 143. N 7. P. 1084–1096.
42. Wei Y., Yang C.R., Wei Y.P., Zhao Z.A., Hou Y., Schatten H., Sun Q.Y. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals // Proc. Natl. Acad. Sci. U S A. 2014. Vol. 111. N 5. P. 1873–1878.
43. Koturbash I., Baker M., Loree J., Kutanzi K., Hudson D., Pogribny I., Sedelnikova O., Bonner W., Kovalchuk O. Epigenetic dysregulation underlies radiation-induced transgenerational genome instability in vivo // Int. J. Radiat. Oncol. Biol. Phys. 2006. Vol. 66. N 2. P. 327–330.
44. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility // Science. 2005. Vol. 308. N 5727. P. 1466–1469.
45. Guerrero-Bosagna C., Settles M., Lucker B., Skinner M.K. Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome // PLoS ONE. 2010. Vol. 5. N 9. e13100.
46. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M.K. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations // PLoS One. 2012. Vol. 7. N 9. e46249.
47. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M.K. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of adult-onset disease and sperm epimutations // PLoS One. 2013. Vol. 8. N 1. e55387.
48. Manikkam M., Haque M.M., Guerrero-Bosagna C., Nilsson E.E., Skinner M.K. Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline // PLoS One. 2014. Vol. 9. N 7. e102091.
49. Skinner M.K., Manikkam M., Tracey R., GuerreroBosagna C., Haque M., Nilsson E.E. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity // BMC Med. 2013. Vol. 11. P. 228.
50. Waldron D. Small RNAs: regulating transgenerational epigenetics // Nat. Rev. Genet. 2016. Vol. 17. N 6. P. 315.
Review
For citations:
Zabuga O.G., Vaiserman A.M. TRANSGENERATIONAL INHERITANCE OF LONGEVITY: THEORETICAL FRAMEWORK AND EMPIRICAL EVIDENCE. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2016;(4):19-27. (In Russ.)