Genetic and Epigenetic Variation, but Not Diet, Shape the Sperm Methylome

Developmental Cell

Volumn 35, Issue 6, 2015, Pages 750-758

  Shea, Jeremy M ^a   Serra, Ryan W ^a   Carone, Benjamin R ^a   Shulha, Hennady P ^a   Kucukural, Alper ^a   Ziller, Michael J ^b,c   Vallaster, Markus P ^a   Gu, Hongcang ^b,c   Tapper, Andrew R ^a   Gardner, Paul D ^a   Meissner, Alexander ^b,c   Garber, Manuel ^a   Rando, Oliver J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b Harvard University   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; RIBOSOME DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DIET; DNA METHYLATION; EPIGENETICS; FEMALE; GENETIC VARIABILITY; HERITABILITY; MALE; METABOLOME; METHYLOME; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPERM; TANDEM REPEAT; ANIMAL; GENETIC EPIGENESIS; GENETIC VARIATION; GENETICS; GENOME; METABOLISM; SPERMATOZOON;

ANIMALS; DIET; DNA METHYLATION; DNA, RIBOSOMAL; EPIGENESIS, GENETIC; EPIGENOMICS; GENETIC VARIATION; GENOME; MALE; MICE; SPERMATOZOA;

EID: 84955280012     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.11.024     Document Type: Article

References (36)

1. Akalin A., Kormaksson M., Li S., Garrett-Bakelman F.E., Figueroa M.E., Melnick A., Mason C.E. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 2012, 13:R87.
2. Aldrich J.C., Maggert K.A. Transgenerational inheritance of diet-induced genome rearrangements in Drosophila. PLoS Genet. 2015, 11:e1005148.
3. Anderson L.M., Riffle L., Wilson R., Travlos G.S., Lubomirski M.S., Alvord W.G. Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 2006, 22:327-331.
4. Bock C., Tomazou E.M., Brinkman A.B., Müller F., Simmer F., Gu H., Jäger N., Gnirke A., Stunnenberg H.G., Meissner A. Quantitative comparison of genome-wide DNA methylation mapping technologies. Nat. Biotechnol. 2010, 28:1106-1114.
5. Boyle P., Clement K., Gu H., Smith Z.D., Ziller M., Fostel J.L., Holmes L., Meldrim J., Kelley F., Gnirke A., Meissner A. Gel-free multiplexed reduced representation bisulfite sequencing for large-scale DNA methylation profiling. Genome Biol. 2012, 13:R92.
6. Carone B.R., Fauquier L., Habib N., Shea J.M., Hart C.E., Li R., Bock C., Li C., Gu H., Zamore P.D., et al. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 2010, 143:1084-1096.
7. Cedar H., Bergman Y. Programming of DNA methylation patterns. Annu. Rev. Biochem. 2012, 81:97-117.
8. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 2012, 13:153-162.
9. Deaton A.M., Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011, 25:1010-1022.
10. Feinberg A.P., Irizarry R.A. Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc. Natl. Acad. Sci. USA 2010, 107(Suppl 1):1757-1764.
11. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
12. Gibbons J.G., Branco A.T., Yu S., Lemos B. Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans. Nat. Commun. 2014, 5:4850.
13. Harris A., Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 2011, 59:279-289.
14. Irizarry R.A., Ladd-Acosta C., Wen B., Wu Z., Montano C., Onyango P., Cui H., Gabo K., Rongione M., Webster M., et al. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet. 2009, 41:178-186.
15. Jimenez-Chillaron J.C., Isganaitis E., Charalambous M., Gesta S., Pentinat-Pelegrin T., Faucette R.R., Otis J.P., Chow A., Diaz R., Ferguson-Smith A., Patti M.E. Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice. Diabetes 2009, 58:460-468.
16. Li M., Sloboda D.M., Vickers M.H. Maternal obesity and developmental programming of metabolic disorders in offspring: evidence from animal models. Exp. Diabetes Res. 2011, 2011:592408.
17. Lumey L.H., Stein A.D., Kahn H.S., van der Pal-de Bruin K.M., Blauw G.J., Zybert P.A., Susser E.S. Cohort profile: the Dutch Hunger Winter families study. Int. J. Epidemiol. 2007, 36:1196-1204.
18. Molaro A., Hodges E., Fang F., Song Q., McCombie W.R., Hannon G.J., Smith A.D. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 2011, 146:1029-1041.
19. Nagy A. Manipulating the Mouse Embryo: A Laboratory Manual 2003, Cold Spring Harbor Laboratory Press. Third Edition.
20. Ng S.F., Lin R.C., Laybutt D.R., Barres R., Owens J.A., Morris M.J. Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 2010, 467:963-966.
21. Paredes S., Branco A.T., Hartl D.L., Maggert K.A., Lemos B. Ribosomal DNA deletions modulate genome-wide gene expression: "rDNA-sensitive" genes and natural variation. PLoS Genet. 2011, 7:e1001376.
22. Pembrey M.E., Bygren L.O., Kaati G., Edvinsson S., Northstone K., Sjöström M., Golding J. Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 2006, 14:159-166. ALSPAC Study Team.
23. Radford E.J., Isganaitis E., Jimenez-Chillaron J., Schroeder J., Molla M., Andrews S., Didier N., Charalambous M., McEwen K., Marazzi G., et al. An unbiased assessment of the role of imprinted genes in an intergenerational model of developmental programming. PLoS Genet. 2012, 8:e1002605.
24. Radford E.J., Ito M., Shi H., Corish J.A., Yamazawa K., Isganaitis E., Seisenberger S., Hore T.A., Reik W., Erkek S., et al. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 2014, 345:1255903.
25. Rando O.J. Daddy issues: paternal effects on phenotype. Cell 2012, 151:702-708.
26. Rando O.J., Simmons R.A. I'm eating for two: parental dietary effects on offspring metabolism. Cell 2015, 161:93-105.
27. Schmitz R.J., Schultz M.D., Lewsey M.G., O'Malley R.C., Urich M.A., Libiger O., Schork N.J., Ecker J.R. Transgenerational epigenetic instability is a source of novel methylation variants. Science 2011, 334:369-373.
28. Shiao Y.H., Crawford E.B., Anderson L.M., Patel P., Ko K. Allele-specific germ cell epimutation in the spacer promoter of the 45S ribosomal RNA gene after Cr(III) exposure. Toxicol. Appl. Pharmacol. 2005, 205:290-296.
29. Shiao Y.H., Leighty R.M., Wang C., Ge X., Crawford E.B., Spurrier J.M., McCann S.D., Fields J.R., Fornwald L., Riffle L., et al. Molecular and organismal changes in offspring of male mice treated with chemical stressors. Environ. Mol. Mutagen. 2012, 53:392-407.
30. Smith Z.D., Chan M.M., Mikkelsen T.S., Gu H., Gnirke A., Regev A., Meissner A. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 2012, 484:339-344.
31. Waterland R.A., Jirtle R.L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 2003, 23:5293-5300.
32. Watkins A.J., Sinclair K.D. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am. J. Physiol. Heart Circ. Physiol. 2014, 306:H1444-H1452.
33. 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. USA 2014, 111:1873-1878.
34. Whitelaw N.C., Whitelaw E. Transgenerational epigenetic inheritance in health and disease. Curr. Opin. Genet. Dev. 2008, 18:273-279.
35. Xi Y., Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 2009, 10:232.
36. Ziller M.J., Hansen K.D., Meissner A., Aryee M.J. Coverage recommendations for methylation analysis by whole-genome bisulfite sequencing. Nat. Methods 2015, 12:230-232.