Transgenerational epigenetic effects on brain functions

Biological Psychiatry

Volumn 73, Issue 4, 2013, Pages 313-320

  Bohacek, Johannes ^a   Gapp, Katharina ^a   Saab, Bechara J ^a   Mansuy, Isabelle M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Disease risk; DNA methylation; epigenetics; germline; histone; inheritance; mechanisms; mental illness; sperm; transgenerational

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AXIN; BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE H3; LYSINE; MICRORNA 1; OXYTOCIN; PROTAMINE; STEM CELL FACTOR RECEPTOR; VINCLOZOLIN;

3' UNTRANSLATED REGION; ANXIETY; BRAIN FUNCTION; CHROMATIN STRUCTURE; DISEASE PREDISPOSITION; DNA METHYLATION; DNA SEQUENCE; ENVIRONMENTAL FACTOR; EPIGENETICS; FERTILIZATION IN VITRO; GERMLINE MICRONUCLEUS; HIPPOCAMPUS; HISTONE MODIFICATION; HUMAN; INHERITANCE; LIFE STRESS; MATERNAL DEPRIVATION; MATERNAL STRESS; NERVE CELL PLASTICITY; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN PROCESSING; RECEPTOR GENE; REPRODUCTION; REVIEW; RNA SPLICING; SPERMATOGENESIS;

BRAIN; DNA METHYLATION; EPIGENESIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INHERITANCE PATTERNS; MENTAL DISORDERS;

EID: 84872849505     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2012.08.019     Document Type: Review

References (100)

1. K.S. Kendler Twin studies of psychiatric illness: An update Arch Gen Psychiatry 58 2001 1005 1014
2. E.E. Eichler, J. Flint, G. Gibson, A. Kong, S.M. Leal, and J.H. Moore Missing heritability and strategies for finding the underlying causes of complex disease Nat Rev Genet 11 2010 446 450
3. M.J. Millan, Y. Agid, M. Brüne, E.T. Bullmore, C.S. Carter, and N.S. Clayton Cognitive dysfunction in psychiatric disorders: Characteristics, causes and the quest for improved therapy Nat Rev Drug Discov 11 2012 141 168
4. E.S. Gershon, N. Alliey-Rodriguez, and C. Liu After GWAS: Searching for genetic risk for schizophrenia and bipolar disorder Am J Psychiatry 168 2011 253 256
5. C.M. Lewis, M.Y. Ng, A.W. Butler, S. Cohen-Woods, R. Uher, and K. Pirlo Genome-wide association study of major recurrent depression in the U.K. population Am J Psychiatry 167 2010 949 957
6. H.-C. So, A.H.S. Gui, S.S. Cherny, and P.C. Sham Evaluating the heritability explained by known susceptibility variants: A survey of ten complex diseases Genetic Epidemiol 35 2011 310 317
7. T.A. Manolio, F.S. Collins, N.J. Cox, D.B. Goldstein, and L.A. Hindorff Finding the missing heritability of complex diseases Nature 461 2009 747 753
8. É. Danchin, A. Charmantier, F.A. Champagne, A. Mesoudi, B. Pujol, and S. Blanchet Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution Nat Rev Genet 12 2011 475 486
9. Bohacek J, Mansuy IM (2012): Epigenetic inheritance of disease and disease risk [published online ahead of print July 11]. Neuropsychopharmacology.
10. J. Tost DNA methylation: An introduction to the biology and the disease-associated changes of a promising biomarker Methods Mol Biol 507 2009 3 20
11. R.Y. Tweedie-Cullen, J.M. Reck, and I.M. Mansuy Comprehensive mapping of post-translational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain J Proteome Res 8 2009 4966 4982
12. MA. Dawson, and T. Kouzarides Cancer epigenetics: From mechanism to therapy Cell 150 2012 12 27
13. M. Ghildiyal, and P.D. Zamore Small silencing RNAs: An expanding universe Nat Rev Genet 10 2009 94 108
14. J.J. Day, and J.D. Sweatt Epigenetic mechanisms in cognition Neuron 70 2011 813 829
15. C. Murgatroyd, A.V. Patchev, Y. Wu, V. Micale, Y. Bockmuhl, and D. Fischer Dynamic DNA methylation programs persistent adverse effects of early-life stress Nat Neurosci 12 2009 1559 1566
16. I.C. Weaver Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: Let's call the whole thing off Epigenetics 2 2007 22 28
17. J. Chen, A.N. Evans, Y. Liu, M. Honda, J.M. Saavedra, and G. Aguilera Maternal deprivation in rats is associated with corticotropin releasing hormone (Crh) promoter hypomethylation and enhances crh transcriptional responses to stress in adulthood J Neuroendocrinol 24 2012 1055 1064
18. A.J. Robison, and E.J. Nestler Transcriptional and epigenetic mechanisms of addiction Nat Rev Neurosci 12 2011 623 637
19. TB. Franklin, and I.M. Mansuy Epigenetic inheritance in mammals: Evidence for the impact of adverse environmental effects Neurobiol Dis 39 2010 61 65
20. C. Guerrero-Bosagna, and M.K. Skinner Environmentally induced epigenetic transgenerational inheritance of phenotype and disease Mol Cell Endocrinol 354 2011 3 8
21. E. Jablonka, and G. Raz Transgenerational epigenetic inheritance: Prevalence, mechanisms, and implications for the study of heredity and evolution Q Rev Biol 84 2009 131 176
22. RL. Jirtle, and M.K. Skinner Environmental epigenomics and disease susceptibility Nat Rev Genet 8 2007 253 262
23. NA. Youngson, and E. Whitelaw Transgenerational epigenetic effects Annu Rev Genomics Hum Genet 9 2008 233 257
24. F.A. Champagne Epigenetic mechanisms and the transgenerational effects of maternal care Front Neuroendocrinol 29 2008 386 397
25. P.O. McGowan, M. Suderman, A. Sasaki, T.C. Huang, M. Hallett, and M.J. Meaney Broad epigenetic signature of maternal care in the brain of adult rats PLoS One 6 2011 e14739
26. I.C. Weaver, N. Cervoni, F.A. Champagne, A.C. D'Alessio, S. Sharma, and J.R. Seckl Epigenetic programming by maternal behavior Nat Neurosci 7 2004 847 854
27. I.C. Weaver, A.C. D'Alessio, S.E. Brown, I.C. Hellstrom, S. Dymov, and S. Sharma The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: Altering epigenetic marks by immediate-early genes J Neurosci 27 2007 1756 1768
28. 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
29. J. Curley, and R. Mashoodh Parent-of-origin and trans-generational germline influences on behavioral development: The interacting roles of mothers, fathers, and grandparents Dev Psychobiol 52 2010 312 330
30. K.S. Grace, and K.D. Sinclair Assisted reproductive technology, epigenetics, and long-term health: A developmental time bomb still ticking Semin Reprod Med 27 2009 409 416
31. J. Weaver, M. Susiarjo, and M. Bartolomei Imprinting and epigenetic changes in the early embryo Mamm Genome 20 2009 532 543
32. P. Hajkova Epigenetic reprogramming in the germline: Towards the ground state of the epigenome Phil Trans R Soc B Biol Sci 366 2011 2266 2273
33. A. Fischer, F. Sananbenesi, A. Mungenast, and L.H. Tsai Targeting the correct HDAC(s) to treat cognitive disorders Trends Pharmacol Sci 31 2010 605 617
34. SA. Krawetz Paternal contribution: New insights and future challenges Nat Rev Genet 6 2005 633 642
35. GD. Johnson, C. Lalancette, A.K. Linnemann, Leduc Fdr, G. Boissonneault, and S.A. Krawetz The sperm nucleus: Chromatin, RNA, and the nuclear matrix Reproduction 141 2011 21 36
36. K. Sha A mechanistic view of genomic imprinting Annu Rev Genomics Hum Genet 9 2008 197 216
37. A. Paoloni-Giacobino, and J. Chaillet The role of DMDs in the maintenance of epigenetic states Cytogenet Genome Res 113 2006 116 121
38. M.S. Bartolomei, and A.C. Ferguson-Smith Mammalian genomic imprinting Cold Spring Harb Perspect Biol 3 2011 a002592
39. S. Feng, S.E. Jacobsen, and W. Reik Epigenetic reprogramming in plant and animal development Science 330 2010 622 627
40. W. Reik, and J. Walter Genomic imprinting: parental influence on the genome Nat Rev Genet 2 2001 21 32
41. J. Borgel, S. Guibert, Y. Li, H. Chiba, D. Schubeler, and H. Sasaki Targets and dynamics of promoter DNA methylation during early mouse development Nat Genet 42 2010 1093 1100
42. C. Guerrero-Bosagna, M. Settles, B. Lucker, and MK. Skinner Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome PLoS One 5 2010 e13100
43. T.B. Franklin, H. Russig, I.C. Weiss, J. Graff, N. Linder, and A. Michalon Epigenetic transmission of the impact of early stress across generations Biol Psychiatry 68 2010 408 415
44. C.C. Oakes, D.J. Smiraglia, C. Plass, JM. Trasler, and B. Robaire Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats Proc Natl Acad Sci 100 2003 1775 1780
45. 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
46. D. Puri, J. Dhawan, and R.K. Mishra The paternal hidden agenda: Epigenetic inheritance through sperm chromatin Epigenetics 5 2010 386 391
47. U. Brykczynska, M. Hisano, S. Erkek, L. Ramos, E.J. Oakeley, and T.C. Roloff Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa Nat Struct Mol Biol 17 2010 679 687
48. T. Hamatani Human spermatozoal RNAs Fertil Steril 97 2012 275 281
49. G.D. Johnson, E. Sendler, C. Lalancette, R. Hauser, M.P. Diamond, and S.A. Krawetz Cleavage of rRNA ensures translational cessation in sperm at fertilization Mol Hum Reprod 17 2011 721 726
50. SA. Krawetz, A. Kruger, C. Lalancette, R. Tagett, E. Anton, and S. Draghici A survey of small RNAs in human sperm Hum Reprod 26 2011 3401 3412
51. N. Suh, and R. Blelloch Small RNAs in early mammalian development: From gametes to gastrulation Development 138 2011 1653 1661
52. D.H. Kim, P. Saetrom, O. Snove Jr, and J.J. Rossi MicroRNA-directed transcriptional gene silencing in mammalian cells Proc Natl Acad Sci U S A 105 2008 16230 16235
53. KV. Morris, S.W.-L. Chan, S.E. Jacobsen, and D.J. Looney Small interfering RNA-induced transcriptional gene silencing in human cells Science 305 2004 1289 1292
54. ST. Younger, and D.R. Corey Transcriptional gene silencing in mammalian cells by miRNA mimics that target gene promoters Nucl Acids Res 39 2011 5682 5691
55. GC. Ostermeier, D. Miller, J.D. Huntriss, M.P. Diamond, and S.A. Krawetz Reproductive biology: Delivering spermatozoan RNA to the oocyte Nature 429 2004 154
56. W.-M. Liu, R.T.K. Pang, P.C.N. Chiu, B.P.C. Wong, K. Lao, and K.-F. Lee Sperm-borne microRNA-34c is required for the first cleavage division in mouse Proc Natl Acad Sci 109 2012 490 494
57. RTK. Pang, W.-M. Liu, C.O.N. Leung, T.-M. Ye, P.C.K. Kwan, and K.-F. Lee miR-135A regulates preimplantation embryo development through down-regulation of e3 ubiquitin ligase seven in absentia homolog 1a (SIAH1A) expression PLoS ONE 6 2011 e27878
58. J.A. Law, and S.E. Jacobsen Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat Rev Genet 11 2010 204 220
59. A.A. Aravin, R. Sachidanandam, D. Bourc'his, C. Schaefer, D. Pezic, and K.F. Toth A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice Mol Cell 31 2008 785 799
60. K.M. Godfrey, P.D. Gluckman, and M.A. Hanson Developmental origins of metabolic disease: Life course and intergenerational perspectives Trends Endocrinol Metab 21 2010 199 205
61. H.D. Morgan, H.G. Sutherland, D.I. Martin, and E. Whitelaw Epigenetic inheritance at the agouti locus in the mouse Nat Genet 23 1999 314 318
62. V.K. Rakyan, S. Chong, M.E. Champ, P.C. Cuthbert, H.D. Morgan, and K.V.K. Luu Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission Proc Natl Acad Sci U S A 100 2003 2538 2543
63. CS. Rosenfeld Animal models to study environmental epigenetics Biol Reprod 82 2010 473 488
64. GL. Wolff, R.L. Kodell, S.R. Moore, and C.A. Cooney Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice FASEB J 12 1998 949 957
65. R. Fernandez-Gonzalez, M.A. Ramirez, E. Pericuesta, A. Calle, and A. Gutierrez-Adan Histone modifications at the blastocyst Axin1Fu locus mark the heritability of in vitro culture-induced epigenetic alterations in mice Biol Reprod 83 2010 720 727
66. 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 U S A 103 2006 17308 17312
67. JE. Cropley, T.H.Y. Dang, D.I.K. Martin, and C.M. Suter The penetrance of an epigenetic trait in mice is progressively yet reversibly increased by selection and environment Proc Biol Sci 279 2012 2375-2353
68. C.C.Y. Li, J.E. Cropley, M.J. Cowley, T. Preiss, D.I.K. Martin, and C.M. Suter A sustained dietary change increases epigenetic variation in isogenic mice PLoS Genet 7 2011 e1001380
69. R.A. Waterland, M. Travisano, and K.G. Tahiliani Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female FASEB J 21 2007 3380 3385
70. K. Delaval, J. Govin, F. Cerqueira, S. Rousseaux, S. Khochbin, and R. Feil Differential histone modifications mark mouse imprinting control regions during spermatogenesis EMBO J 26 2007 720 729
71. C. Heim, D.J. Newport, T. Mletzko, A.H. Miller, and C.B. Nemeroff The link between childhood trauma and depression: Insights from HPA axis studies in humans Psychoneuroendocrinology 33 2008 693 710
72. T.B. Franklin, N. Linder, H. Russig, B. Thöny, and I.M. Mansuy Influence of early stress on social abilities and serotonergic functions across generations in mice PLoS One 6 2011 e21842
73. I.C. Weiss, T.B. Franklin, S. Vizi, and I.M. Mansuy Inheritable effect of unpredictable maternal separation on behavioral responses in mice Front Behav Neurosci 2011 doi:10.3389/fnbeh.2011.00003
74. T.L. Roth, F.D. Lubin, A.J. Funk, and J.D. Sweatt Lasting epigenetic influence of early-life adversity on the BDNF gene Biol Psychiatry 65 2009 760 769
75. C.P. Morgan, and T.L. Bale Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage J Neurosci 31 2011 11748 11755
76. D.M. Dietz, Q. LaPlant, E.L. Watts, G.E. Hodes, S.J. Russo, and J. Feng Paternal transmission of stress-induced pathologies Biol Psychiatry 70 2011 408 414
77. M.K. Skinner, MD. Anway, M.I. Savenkova, A.C. Gore, and D. Crews Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior PLoS One 3 2008 e3745
78. D. Crews, R. Gillette, S.V. Scarpino, M. Manikkam, M.I. Savenkova, and M.K. Skinner Epigenetic transgenerational inheritance of altered stress responses Proc Natl Acad Sci 109 2012 9143 9148
79. C. Stouder, and A. Paoloni-Giacobino Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm Reproduction 139 2010 373 379
80. J.T. Wolstenholme, M. Edwards, S.R.J. Shetty, J.D. Gatewood, J.A. Taylor, and E.F. Rissman Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression Endocrinology 153 2012 3828 3838
81. K. Sato, H. Fukata, Y. Kogo, J. Ohgane, K. Shiota, and C. Mori Neonatal exposure to diethylstilbestrol alters expression of dna methyltransferases and methylation of genomic DNA in the mouse uterus Endocr J 56 2009 131 139
82. BE. Walker Tumors of female offspring of mice exposed prenatally to diethylstilbestrol J Natl Cancer Inst 73 1984 133 140
83. R.R. Newbold, E. Padilla-Banks, and W.N. Jefferson Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations Endocrinology 147 2006 s11 s17
84. J.G. Bromer, J. Wu, Y. Zhou, and H.S. Taylor Hypermethylation of Homeobox A10 by in utero diethylstilbestrol exposure: An epigenetic mechanism for altered developmental programming Endocrinology 150 2009 3376 3382
85. S. Li, K.A. Washburn, R. Moore, T. Uno, C. Teng, and R.R. Newbold Developmental exposure to diethylstilbestrol elicits demethylation of estrogen-responsive lactoferrin gene in mouse uterus Cancer Res 57 1997 4356 4359
86. K.L. Bruner-Tran, and K.G. Osteen Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations Reprod Toxicol 31 2011 344 350
87. J. Simpson, and J.P. Kelly The impact of environmental enrichment in laboratory rats: Behavioural and neurochemical aspects Behav Brain Res 222 2011 246 264
88. J. Nithianantharajah, and A.J. Hannan Enriched environments, experience-dependent plasticity and disorders of the nervous system Nat Rev Neurosci 7 2006 697 709
89. J.A. Arai, S. Li, D.M. Hartley, and L.A. Feig Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment J Neurosci 29 2009 1496 1502
90. 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
91. K.D. Wagner, N. Wagner, H. Ghanbarian, V. Grandjean, P. Gounon, and F. Cuzin RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse Dev Cell 14 2008 962 969
92. L.V. Harper Epigenetic inheritance and the intergenerational transfer of experience Psychol Bull 131 2005 340 360
93. P.D. Gluckman, M.A. Hanson, P. Bateson, A.S. Beedle, C.M. Law, and Z.A. Bhutta Towards a new developmental synthesis: Adaptive developmental plasticity and human disease Lancet 373 2009 1654 1657
94. C. Hales, and D. Barker Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis Diabetologia 35 1992 595 601
95. A.M. Brunner, R.Y. Tweedie-Cullen, and I.M. Mansuy Epigenetic modifications of the neuroproteome Proteomics 12 2012 2404 2420
96. M. Rodriguez-Paredes, and M. Esteller Cancer epigenetics reaches mainstream oncology Nat Med 2011 330 339
97. H.E. Covington III, I. Maze, Q.C. LaPlant, V.F. Vialou, Y.N. Ohnishi, and O. Berton Antidepressant actions of histone deacetylase inhibitors J Neurosci 29 2009 11451 11460
98. J. Graff, D. Rei, J.-S. Guan, W.-Y. Wang, J. Seo, and K.M. Hennig An epigenetic blockade of cognitive functions in the neurodegenerating brain Nature 483 2012 222 226
99. P. Narayan, and M. Dragunow Pharmacology of epigenetics in brain disorders Br J Pharmacol 159 2010 285 303
100. C.H. Arrowsmith, C. Bountra, P.V. Fish, K. Lee, and M. Schapira Epigenetic protein families: A new frontier for drug discovery Nat Rev Drug Discov 11 2012 384 400