Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals

Cell

Volumn 143, Issue 7, 2010, Pages 1084-1096

  Carone, Benjamin R ^a   Fauquier, Lucas ^a   Habib, Naomi ^c,d   Shea, Jeremy M ^a   Hart, Caroline E ^a   Li, Ruowang ^b   Bock, Christoph ^e,f   Li, Chengjian ^a   Gu, Hongcang ^e   Zamore, Phillip D ^a,b   Meissner, Alexander ^e,f   Weng, Zhiping ^b   Hofmann, Hans A ^g   Friedman, Nir ^c   Rando, Oliver J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

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

^f Harvard University   (United States)

^g UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DNA METHYLATION; DNA MODIFICATION; ENVIRONMENTAL FACTOR; FATHER CHILD RELATION; GENE EXPRESSION; HEREDITY; LIPOGENESIS; MALE; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN RESTRICTION;

MAMMALIA; MUS;

EID: 78650446334     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.12.008     Document Type: Article

References (69)

1. L.M. Anderson, L. Riffle, R. Wilson, G.S. Travlos, M.S. Lubomirski, and W.G. Alvord Preconceptional fasting of fathers alters serum glucose in offspring of mice Nutrition 22 2006 327 331
2. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science 308 2005 1466 1469
3. A. Arpanahi, M. Brinkworth, D. Iles, S.A. Krawetz, A. Paradowska, A.E. Platts, M. Saida, K. Steger, P. Tedder, and D. Miller Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences Genome Res. 19 2009 1338 1349
4. E. Avital, and E. Jablonka Animal Traditions: Behavioural Inheritance in Evolution 2000 Cambridge University Press Cambridge, UK
5. M.S. Bartolomei, A.L. Webber, M.E. Brunkow, and S.M. Tilghman Epigenetic mechanisms underlying the imprinting of the mouse H19 gene Genes Dev. 7 1993 1663 1673
6. M.E. Blewitt, N.K. Vickaryous, A. Paldi, H. Koseki, and E. Whitelaw Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice PLoS Genet. 2 2006 e49
7. W.H. Boylston, A. Gerstner, J.H. DeFord, M. Madsen, K. Flurkey, D.E. Harrison, and J. Papaconstantinou Altered cholesterologenic and lipogenic transcriptional profile in livers of aging Snell dwarf (Pit1dw/dwJ) mice Aging Cell 3 2004 283 296
8. U. Brykczynska, M. Hisano, S. Erkek, L. Ramos, E.J. Oakeley, T.C. Roloff, C. Beisel, D. Schubeler, M.B. Stadler, and A.H. Peters Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa Nat. Struct. Mol. Biol. 17 2010 679 687
9. F. Champagne, and M.J. Meaney Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity Prog. Brain Res. 133 2001 287 302
10. S. Chong, N. Vickaryous, A. Ashe, N. Zamudio, N. Youngson, S. Hemley, T. Stopka, A. Skoultchi, J. Matthews, and H.S. Scott Modifiers of epigenetic reprogramming show paternal effects in the mouse Nat. Genet. 39 2007 614 622
11. D. Crews, A.C. Gore, T.S. Hsu, N.L. Dangleben, M. Spinetta, T. Schallert, M.D. Anway, and M.K. Skinner Transgenerational epigenetic imprints on mate preference Proc. Natl. Acad. Sci. USA 104 2007 5942 5946
12. J.E. Cropley, C.M. Suter, K.B. Beckman, and D.I. Martin Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation Proc. Natl. Acad. Sci. USA 103 2006 17308 17312
13. M. Diehn, A.A. Alizadeh, O.J. Rando, C.L. Liu, K. Stankunas, D. Botstein, G.R. Crabtree, and P.O. Brown Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation Proc. Natl. Acad. Sci. USA 99 2002 11796 11801
14. C. Fricke, A. Bretman, and T. Chapman Adult male nutrition and reproductive success in Drosophila melanogaster Evolution 62 2008 3170 3177
15. M. Ghildiyal, H. Seitz, M.D. Horwich, C. Li, T. Du, S. Lee, J. Xu, E.L. Kittler, M.L. Zapp, and Z. Weng Endogenous siRNAs derived from transposons and mRNAs in Drosophila somatic cells Science 320 2008 1077 1081
16. S. Gray, B. Wang, Y. Orihuela, E.G. Hong, S. Fisch, S. Haldar, G.W. Cline, J.K. Kim, O.D. Peroni, and B.B. Kahn Regulation of gluconeogenesis by Kruppel-like factor 15 Cell Metab. 5 2007 305 312
17. C.N. Hales, and D.J. Barker The thrifty phenotype hypothesis Br. Med. Bull. 60 2001 5 20
18. S.S. Hammoud, D.A. Nix, H. Zhang, J. Purwar, D.T. Carrell, and B.R. Cairns Distinctive chromatin in human sperm packages genes for embryo development Nature 460 2009 473 478
19. A. Harris, and J. Seckl Glucocorticoids, prenatal stress and the programming of disease Horm. Behav. 2010 10.1016/j.yhbeh.2010.06.007 Published online June 18, 2010
20. B.T. Heijmans, E.W. Tobi, A.D. Stein, H. Putter, G.J. Blauw, E.S. Susser, P.E. Slagboom, and L.H. Lumey Persistent epigenetic differences associated with prenatal exposure to famine in humans Proc. Natl. Acad. Sci. USA 105 2008 17046 17049
21. N.D. Heintzman, R.K. Stuart, G. Hon, Y. Fu, C.W. Ching, R.D. Hawkins, L.O. Barrera, S. Van Calcar, C. Qu, and K.A. Ching Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome Nat. Genet. 39 2007 311 318
22. D.G. Hendrickson, D.J. Hogan, D. Herschlag, J.E. Ferrell, and P.O. Brown Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance PLoS ONE 3 2008 e2126
23. R. Holliday The inheritance of epigenetic defects Science 238 1987 163 170
24. J.D. Horton, N.A. Shah, J.A. Warrington, N.N. Anderson, S.W. Park, M.S. Brown, and J.L. Goldstein Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes Proc. Natl. Acad. Sci. USA 100 2003 12027 12032
25. T.H. Horton Fetal origins of developmental plasticity: animal models of induced life history variation Am. J. Hum. Biol. 17 2005 34 43
26. E. Jablonka, and M.J. Lamb Epigenetic Inheritance and Evolution: The Lamarckian Dimension 1995 Oxford University Press Oxford, UK
27. E. Jablonka, and M.J. Lamb Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life 2005 MIT Press Cambridge, MA
28. F.V. Jacinto, E. Ballestar, and M. Esteller Methyl-DNA immunoprecipitation (MeDIP): hunting down the DNA methylome Biotechniques 44 2008 35, 37, 39 passim
29. T. Jerome, P. Laurie, B. Louis, and C. Pierre Enjoy the silence: the story of let-7 microRNA and cancer Curr. Genomics 8 2007 229 233
30. J. Jiang, Y. Gusev, I. Aderca, T.A. Mettler, D.M. Nagorney, D.J. Brackett, L.R. Roberts, and T.D. Schmittgen Association of microRNA expression in hepatocellular carcinomas with hepatitis infection, cirrhosis, and patient survival Clin. Cancer Res. 14 2008 419 427
31. G. Kaati, L.O. Bygren, and S. Edvinsson Cardiovascular and diabetes mortality determined by nutrition during parents' and grandparents' slow growth period Eur. J. Hum. Genet. 10 2002 682 688
32. L. Lumey, A.D. Stein, H.S. Kahn, K.M. van der Pal-de Bruin, G. Blauw, P.A. Zybert, and E.S. Susser Cohort profile: the Dutch hunger winter families study Int. J. Epidemiol. 36 2007 1196 1204
33. M.A. Madsen, C.C. Hsieh, W.H. Boylston, K. Flurkey, D. Harrison, and J. Papaconstantinou Altered oxidative stress response of the long-lived Snell dwarf mouse Biochem. Biophys. Res. Commun. 318 2004 998 1005
34. M.J. Meaney, M. Szyf, and J.R. Seckl Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health Trends Mol. Med. 13 2007 269 277
35. A. Meissner, T.S. Mikkelsen, H. Gu, M. Wernig, J. Hanna, A. Sivachenko, X. Zhang, B.E. Bernstein, C. Nusbaum, and D.B. Jaffe Genome-scale DNA methylation maps of pluripotent and differentiated cells Nature 454 2008 766 770
36. T. Moore, and D. Haig Genomic imprinting in mammalian development: a parental tug-of-war Trends Genet. 7 1991 45 49
37. S.F. Ng, R.C. Lin, D.R. Laybutt, R. Barres, J.A. Owens, and M.J. Morris Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring Nature 467 2010 963 966
38. S.L. Ooi, and S. Henikoff Germline histone dynamics and epigenetics Curr. Opin. Cell Biol. 19 2007 257 265
39. M.E. Pembrey, L.O. Bygren, G. Kaati, S. Edvinsson, K. Northstone, M. Sjostrom, and J. Golding Sex-specific, male-line transgenerational responses in humans Eur. J. Hum. Genet. 14 2006 159 166
40. S.R. Pryke, and S.C. Griffith Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch Science 323 2009 1605 1607
41. M. Rakhshandehroo, L.M. Sanderson, M. Matilainen, R. Stienstra, C. Carlberg, P.J. de Groot, M. Muller, and S. Kersten Comprehensive analysis of PPARalpha-dependent regulation of hepatic lipid metabolism by expression profiling PPAR Res. 2007 2007 26839
42. V.K. Rakyan, S. Chong, M.E. Champ, P.C. Cuthbert, H.D. Morgan, K.V. Luu, and E. Whitelaw Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission Proc. Natl. Acad. Sci. USA 100 2003 2538 2543
43. O.J. Rando, and K.J. Verstrepen Timescales of genetic and epigenetic inheritance Cell 128 2007 655 668
44. M. Rassoulzadegan, V. Grandjean, P. Gounon, S. Vincent, I. Gillot, and F. Cuzin RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse Nature 441 2006 469 474
45. M.E. Symonds, S.P. Sebert, M.A. Hyatt, and H. Budge Nutritional programming of the metabolic syndrome Nat. Rev. Endocrinol. 5 2009 604 610
46. T. Tsuchiya, J.M. Dhahbi, X. Cui, P.L. Mote, A. Bartke, and S.R. Spindler Additive regulation of hepatic gene expression by dwarfism and caloric restriction Physiol. Genomics 17 2004 307 315
47. K.D. Wagner, N. Wagner, H. Ghanbarian, V. Grandjean, P. Gounon, F. Cuzin, and M. Rassoulzadegan RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse Dev. Cell 14 2008 962 969
48. R.A. Waterland, and R.L. Jirtle Transposable elements: targets for early nutritional effects on epigenetic gene regulation Mol. Cell. Biol. 23 2003 5293 5300
49. I.C. Weaver, N. Cervoni, F.A. Champagne, A.C. D'Alessio, S. Sharma, J.R. Seckl, S. Dymov, M. Szyf, and M.J. Meaney Epigenetic programming by maternal behavior Nat. Neurosci. 7 2004 847 854
50. M. Weber, J.J. Davies, D. Wittig, E.J. Oakeley, M. Haase, W.L. Lam, and D. Schubeler Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells Nat. Genet. 37 2005 853 862
51. M. Weber, I. Hellmann, M.B. Stadler, L. Ramos, S. Paabo, M. Rebhan, and D. Schubeler Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome Nat. Genet. 39 2007 457 466
52. N.C. Whitelaw, and E. Whitelaw Transgenerational epigenetic inheritance in health and disease Curr. Opin. Genet. Dev. 18 2008 273 279
53. M.F. Wolfner The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila Heredity 88 2002 85 93
54. R. Yamaguchi, Y. Nakagawa, Y.J. Liu, Y. Fujisawa, S. Sai, E. Nagata, S. Sano, E. Satake, R. Matsushita, and T. Nakanishi Effects of maternal high-fat diet on serum lipid concentration and expression of peroxisomal proliferator-activated receptors in the early life of rat offspring Horm. Metab. Res. 42 2010 821 825
55. X. Yang, J.L. Deignan, H. Qi, J. Zhu, S. Qian, J. Zhong, G. Torosyan, S. Majid, B. Falkard, and R.R. Kleinhanz Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks Nat. Genet. 41 2009 415 423
56. N.A. Youngson, and E. Whitelaw Transgenerational epigenetic effects Annu. Rev. Genomics Hum. Genet. 9 2008 233 257
57. de Hoon, M.J., Imoto, S., Nolan, J., and Miyano, S. (2004). Open source clustering software. Bioinformatics 20, 1453-1454.
58. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863-14868.
59. Friedlander, M.R., Chen, W., Adamidi, C., Maaskola, J., Einspanier, R., Knespel, S., and Rajewsky, N. (2008). Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26, 407-415.
60. Friedman, R.C., Farh, K.K., Burge, C.B., and Bartel, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105.
61. Horton, J.D., Shah, N.A., Warrington, J.A., Anderson, N.N., Park, S.W., Brown, M.S., and Goldstein, J.L. (2003). Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc. Natl. Acad. Sci. USA 100, 12027-12032.
62. Liu, C.L., Kaplan, T., Kim, M., Buratowski, S., Schreiber, S.L., Friedman, N., and Rando, O.J. (2005). Single-nucleosome mapping of histone modifications in S. cerevisiae. PLoS Biol. 3, e328.
63. Meissner, A., Mikkelsen, T.S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B.E., Nusbaum, C., Jaffe, D.B., et al. (2008). Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
64. Miller, B.H., McDearmon, E.L., Panda, S., Hayes, K.R., Zhang, J., Andrews, J.L., Antoch, M.P., Walker, J.R., Esser, K.A., Hogenesch, J.B., et al. (2007). Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc. Natl. Acad. Sci. USA 104, 3342-3347.
65. Odom, D.T., Dowell, R.D., Jacobsen, E.S., Gordon, W., Danford, T.W., MacIsaac, K.D., Rolfe, P.A., Conboy, C.M., Gifford, D.K., and Fraenkel, E. (2007). Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat. Genet. 39, 730-732.
66. Waterston, R.H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J.F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P., et al. (2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562.
67. Weber, M., Davies, J.J., Wittig, D., Oakeley, E.J., Haase, M., Lam, W.L., and Schubeler, D. (2005). Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat. Genet. 37, 853-862.
68. Weber, M., Hellmann, I., Stadler, M.B., Ramos, L., Paabo, S., Rebhan, M., and Schubeler, D. (2007). Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet. 39, 457-466.
69. Yang, X., Deignan, J.L., Qi, H., Zhu, J., Qian, S., Zhong, J., Torosyan, G., Majid, S., Falkard, B., Kleinhanz, R.R., et al. (2009). Validation of candidate causal genes for obesity that affect shared metabolic pathways and networks. Nat. Genet. 41, 415-423.