Transgenerational genetic effects

Epigenomics

Volumn 2, Issue 6, 2010, Pages 797-806

  Nelson, Vicki R ^a   Nadeau, Joseph H ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

epigenetics; heritability; transgenerational

Indexed keywords

CYCLIN DEPENDENT KINASE 9; MITOGEN ACTIVATED PROTEIN KINASE; RNA; STAT PROTEIN; STEM CELL FACTOR RECEPTOR;

DNA METHYLATION; ENVIRONMENTAL EXPOSURE; GENE DELETION; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; GENETIC ANALYSIS; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; HEREDITY; HETEROCHROMATIN; HUMAN; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; REVIEW; Y CHROMOSOME;

ANIMALS; EPIGENESIS, GENETIC; EPISTASIS, GENETIC; GENE-ENVIRONMENT INTERACTION; GENETIC VARIATION; HUMANS; INHERITANCE PATTERNS; MICE; PHENOTYPE;

EID: 78650452937     PISSN: 17501911     EISSN: 1750192X     Source Type: Journal    
DOI: 10.2217/epi.10.57     Document Type: Review

References (108)

1. Calin GA, Liu CG, Ferracin M et al.: Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell 12(3), 215-229 (2007)
2. Mayr E: The Growth of Biological Thought: Diversity, Evolution and Inheritance. Harvard University Press, Cambridge, UK (1982).
3. Mendel G: Versuche über pflanzen-hybriden. Verhandlungen des Naturforschenden Vereines in Brünn 3-47 (1866).
4. Monaghan F, Corcos A: On the origins of the Mendelian laws. J. Hered. 75, 67-69 (1984).
5. Galton F: Co-relations and their measurement. Proc. R. Soc. 45, 135-145 (1888).
6. Morgan TH: Sex-limited inheritance in Drosophila. Science 32, 120-122 (1910).
7. Sturtevant AH, Bridges CB, Morgan TH: The spatial relations of genes. Proc. Natl Acad. Sci. USA 5, 168-173 (1919).
8. Sturtevant AH: Linkage variation and chromosome maps. Proc. Natl Acad. Sci. USA 7, 181-183 (1921).
9. Avery OT, Macleod CM, McCarty M: Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a deoxyribonucleic acid fraction isolated from Pneumococcus Type III. J. Exp. Med. 79, 137-158 (1944).
10. Hershey AD, Chase M: Independent functions of viral protein and nucleic acid in growth of bacteriophage. J. Genet. Psychol. 36, 39-56 (1952).
11. Fisher RA: On the correlation between relatives on the supposition of Mendelian inheritance. Trans. Roy. Soc. Edinburgh 52, 399-433 (1918).
12. Altshuler D, Daly MJ, Lander ES: Genetic mapping in human disease. Science 322, 881-888 (2008).
13. Manolio TA, Collins FS, Cox NJ et al.: Finding the missing heritability of complex diseases. Nature 461, 747-753 (2009).
14. Clarke AJ, Cooper DN: GWAS: heritability missing in action? Eur. J. Hum. Genet. 18, 859-861 (2010).
15. Slatkin M: Epigenetic inheritance and the missing heritability problem. Genetics 182, 845-850 (2009).
16. Rakyan VK, Preis J, Morgan HD, Whitelaw E: The marks, mechanisms and memory of epigenetic states in mammals. Biochem. J. 356, 1-10 (2001).
17. Darwin C: The Variation in Animals and Plants under Domestication. Murray J (Ed.). John Murray, UK (1868).
18. Lamarck J-B: Recherches sur losorganisation des Corps Vivants. Paris, France (1802).
19. Weismann A: Studien sur Descendants-Theorie. II. Uber die Letzten Ursachen der Transmutationen. Verlag von Wilhelm Engelmann, Leipzig, Germany (1876).
20. Weismann A: Die Entstehung der Sexualzellen bei den Hydromedusan: Zugleich ein beitrag zur kenntniss des baues und der lebenserscheinungen dieser gruppe. Fischer, Jena, Germany (1883).
21. Weismann A: Die Continuitat des Keimplasmas als Grundlage einer Theorie der Vererbung. Fischer, Jena (1885).
22. Gluckman PD, Hanson MA, Beedle AS: Non-genomic transgenerational inheritance of disease risk. Bioessays 29, 145-154 (2007).
23. Jirtle RL, Skinner MK: Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8, 253-262 (2007).
24. Johannes F, Porcher E, Teixeira FK et al.: Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 5, E1000530 (2009).
25. Youngson NA, Whitelaw E: Transgenerational epigenetic effects. Ann. Rev. Genom. Hum. Genet. 9, 233-257 (2008).
26. Alcazar RM, Rueyling L, Fire AZ: Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 180, 1275-1288 (2008).
27. Grishok A Tabara H, Mello CC: Genetic requirements for inheritance of RNAi in C. elegans. Science 287, 2494-2497 (2000).
28. Anway MD, Skinner MK: Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147, S43-S49 (2006).
29. Morgan D, Whitelaw E: The case for transgenerational epigenetic inheritance in humans. Mamm. Genome 19, 394-397 (2008).
30. Rakyan VK, Beck S: Epigenetic variation and inheritance in mammals. Curr. Opin. Genet. Dev. 16, 573-577 (2006).
31. Richards EJ: Inherited epigenetic variation - revisiting soft inheritance. Nat. Rev. Genet. 7, 395-401 (2006).
32. Anway MD, Cupp AS, Uzumcu M, Skinner MK: Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466-1469 (2005).
33. Newbold RR, Padilla-Banks E, Jefferson WN: Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147, S11-S17 (2006).
34. Cheng RY-S, Hockman T, Crawford E, Anderson LM, Shiao Y-H: Epigenetic and gene expression changes related to transgenerational carcinogenesis. Mol. Carcinog. 40, 1-11 (2004).
35. Grenier L, Robaire B, Hales BF: Paternal exposure to cyclophosphamide affects the progression of sperm chromatin decondensation and activates a DNA damage response in prepronuclear rat zygotes. Biol. Reprod. 83, 195-204 (2010).
36. Dent P, Yacoub A, Contessa J et al.: Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat. Res. 159, 283-300 (2003).
37. Wiley LM, Baulch JE, Raabe OG, Straume T: Impaired cell proliferation in mice persists across at least two generations after paternal irradiation. Radiat. Res. 148, 145-151 (1997).
38. Straume T, Raabe OG, Walsh KJ, Wiley LM: Inherited effects from irradiated mouse immature oocytes detected in aggregation embryo chimeras. Mutat. Res. 287, 243-251 (1993).
39. Warner P, Wiley LM, Oudiz DJ, Overstreet JVV, Raabe OG: Paternally inherited effects of g-radiation on mouse preimplantation development detected by the chimera assay. Radiat. Res. 128, 48-58 (1991).
40. Vance MM, Baulch JE, Raabe OG, Wiley LM, Overstreet JW: Cellular reprogramming in the F3 mouse with paternal F0 radiation history. Int. J. Radiat. Biol. 78, 513-526 (2002).
41. Baulch JE, Raabe OG, Wiley LM: Heritable effects of paternal irradiation in mice on signaling protein kinase activities in F3 offspring. Mutagenesis 16, 17-23 (2001).
42. Baulch JE, Raabe OG: g irradiation of Type B speratogonia leads to heritable genomic instability in four generations of mice. Mutagenesis 20, 337-343 (2005).
43. Baulch JE, Li M-W, Raabe OG: Effect of ATM heterozygosity on heritable DNA damage in mice following paternal F0 germline irradiation. Mutat. Res. 616, 34-45 (2007).
44. Dubrova YE: Radiation-induced transgenerational instability. Oncogene 22, 7087-7093 (2003).
45. Dubrova YE: Genomic instability in the offspring of irradiated parents: facts and interpretations. Genetika 42, 1335-1347 (2006).
46. Vorobtsova IE: Transgenerational transmission of radiation induced genomic instability. Radiats. Biol. Radioecol. 46, 441-446 (2006).
47. Kovalchuk O, Baulch JE: Epigenetic and nontargeted radiation effects - is there a link? Environ. Mol. Mutagen. 49, 16-25 (2008).
48. Filkowski JN, Ilnytskyy Y, Tamminga J et al.: Hypomethylation and genome instability in the germline of exposed parents and their progeny is associated with altered miRNA expression. Carcinogenesis 31, 1110-1115 (2010).
49. Burdge GC, Slater-Jefferies J, Torrens C et al.: Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br. J. Nutr. 97, 435-439 (2007).
50. Weaver ICG, Cervoni N, Champagne FA et al.: Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854 (2004).
51. Arai JA, Li S, Hartley DM, Feig LA: Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment. J. Neurosci. 29, 1496-1502 (2009).
52. Kiyono S, Seo ML, Shibagaki M, Inouye M: Facilitative effects of maternal environmental enrichment on maze learning in rat offspring. Physiol. Behav. 34, 431-435 (1985).
53. Curley JP, Davidson S, Bateson P, Champagne FA: Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Front. Behav. Neurosci. 3, 25 (2009).
54. Kaati G, Bygren LO, Pembrey M, Sjostrom M: Transgenerational response to nutrition, early life circumstances and longevity. Eur. J. Hum. Genet. 15, 784-790 (2007).
55. Pembrey ME, Bygren LO, Kaati G et al.: Sex-specific, male-line transgenerational responses in humans. Eur. J. Hum. Genet. 14, 159-66 (2006).
56. Painter R, Osmond C, Gluckman P et al.: Transgenerational effects of prenatal exposure to the Dutch famine in neonatal adiposity and health in later life. BJOG 115, 1243-1249 (2008).
57. Skinner MK, Manikkam M, Guerrero-Bosagna C: Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab. 21, 214-222 (2010).
58. Rassoulzadegan M, Grandjean V, Gounon P et al.: RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature 441, 469-474 (2006).
59. Wandzioch E, Edling CE, Palmer RH, Carlsson L, Hallberg B: Activation of the MAP kinase pathway by c-Kit is PI-3 kinase dependent in hematopoietic progenitor/stem cell lines. Blood 104, 51-57 (2004).
60. Linnekin D: Early signaling pathways activated by c-Kit in hematopoietic cells. Int. J. Biochem. Cell Biol. 31, 1053-1074 (1999).
61. Reith AD, Ellis C, Lyman SD et al.: Signal transduction by normal isoforms and W mutant variants of the Kit receptor tyrosine kinase. EMBO J. 10, 2451-2459 (1991).
62. Weiler S, Mou S, Deberry C et al.: JAK2 is associated with the c-kit proto-oncogene product and is phosphorylated in response to stem cell factor. Blood 87, 3688-3693 (1996). (Pubitemid 26129596)
63. Rönnstrand L: Signal transduction via the stem cell factor receptor/c-Kit. Cell. Mol. Life Sci. 61, 2535-2548 (2004).
64. Edling CE, Hallberg B: c-Kit - a hematopoietic cell essential receptor tyrosine kinase. Int. J. Biochem. Cell Biol. 39, 1995-1998 (2007).
65. Munugalavadla V, Kapur R: Role of c-Kit and erythropoietin receptor in erythropoiesis. Crit. Rev. Oncol. Hematol. 54, 63-75 (2005).
66. Ashman LK: The biology of stem cell factor and its receptor c-kit. Int. J. Biochem. Cell Biol. 31, 1037-1051 (1999).
67. Roskoski R Jr: Signaling by Kit protein-tyrosine kinase - the stem cell factor receptor. Biochem. Biophys. Res. Commun. 337, 1-13 (2005). (Pubitemid 41393751)
68. Arteaga-Vazquez MA, Chandler VL: Paramutation in maize: RNA mediated trans-generational gene silencing. Curr. Opin. Genet. Dev. 20, 156-163 (2010).
69. Chandler VL, Alleman M: Paramutation: epigenetic instructions passed across generations. Genetics 178, 1839-1844 (2008).
70. Rassoulzadegan M, Grandjean V, Gounon P, Cuzin F: Inheritance of an epigenetic change in the mouse: a new role for RNA. Biochem. Soc. Trans. 035, 623-625 (2007).
71. Grandjean V, Gounon P, Wagner N et al.: The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development 136, 3647-3655 (2009).
72. Wagner KD, Wagner N, Ghanbarian H et al.: RNA Induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev. Cell. 14, 962-969 (2008).
73. Heaney JD, Lam M-YJ, Michelson MV, Nadeau JH: Loss of the transmembrane but not the soluble Kit ligand isoform increases testicular germ cell tumor susceptibility in mice. Cancer Res. 68, 5193-5197 (2008).
74. Wolff GL, Kodell RL, Moore SR, Cooney CA: Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 12, 949-957 (1998).
75. Cooney CA, Dave AA, Wolff GL: Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 132, S2393-S2400 (2002).
76. Rakyan VK, Chong S, Champ ME et al.: Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission. Proc. Natl. Acad. Sci USA 100, 2538-2543 (2003).
77. Waterland RA, Dolinoy DC, Lin, J-R, Smith CA, Shi X, Tahiliani KG: Maternal methyl supplements increase offspring DNA methylation at Axin fused. Genesis 44, 401-406 (2006).
78. Bourchis D, Bestor TH: Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99 (2004).
79. Parkhurst SM, Ish-Horowicz D: Wimp, a dominant maternal-effect mutation, reduces transcription of a specific subset of segmental genes in Drosophila. Genes Dev. 5, 341-357 (1991).
80. Xing Y, Shi S, Le L et al. Evidence for transgenerational transmission of epigenetic tumor susceptibility in Drosophila. PLoS Genet. 3, E151 (2007).
81. Lam M-YJ, Heaney JD, Youngren KK et al.: Trans-generational epistasis between Dnd1Ter and other modifier genes controls susceptibility to testicular germ cell tumors. Hum. Mol. Genet. 16, 2233-2240 (2007).
82. Lam M-YJ, Youngren KK, Nadeau JH: Enhancers and suppressors of testicular cancer susceptibility in single-and double-mutant mice. Genetics 166, 925-933 (2004).
83. Petersen-Mahrt SK, Neuberger MS: In vitro deamination of cytosine to uracil in single-stranded DNA by apolipoprotein B editing complex catalytic subunit 1 (APOBEC1). J. Biol. Chem. 278, 19583-19586 (2003).
84. Kedde M, Strasser MJ, Boldajipour B et al.: RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273-1286 (2007).
85. Noguchi T, Noguchi M: A recessive mutation (ter) causing germ cell deficiency and a high incidence of congenital testicular teratomas in 129/Sv-ter mice. J. Natl Cancer Inst. 75, 385-392 (1985).
86. Noguchi T, Stevens LC: Primordial germ cell proliferation in fetal testes in mouse strains with high and low incidences of congenital testicular teratomas. J. Natl Cancer Inst. 69, 907-913 (1982).
87. Nelson VR, Shao H, Nadeau JH: Transgenerational genetic effects of the paternal Y chromosome on daughters phenotypes. Epigenomics 2, 513-521 (2010).
88. Nadeau JH, Singer JB, Matin A, Lander ES: Analyzing complex genetic traits with chromosome substitution strains. Nat. Genet. 24, 221-225 (2000).
89. Yazbek SN, Spiezio SH, Nadeau JH, Buchner DA: Ancestral paternal genotype determines diet-induced obesity and food intake for multiple generations. Hum. Mol. Genet. 19(21), 4134-4144 (2010).
90. Ng SF, Lin RCY, Laybutt DR et al.: Chronic high-fat diet in fathers programs b-cell dysfunction in female rat offspring. Nature 467, 963-967 (2010).
91. Alcazar RM, Rueyling L, Fire AZ: Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 180, 1275-1288 (2008)
92. Carmell MA, Girard A, van de Kant HJG et al.: MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Develop. Cell. 12, 503-514 (2007).
93. Farthing CR, Ficz G, Ng RK et al.: Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, E1000116 (2008).
94. Brykczynska U, Hisano M, Erkek S et al.: Repressive and active methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687 (2010).
95. Guilbert S, Forne T, Weber M: Dynamic regulation of DNA methylation during mammalian development. Epigenomics 1, 81-98 (2009).
96. Grishok A Tabara H, Mello CC: Genetic requirements for inheritance of RNAi in C. elegans. Science 287, 2494-2497 (2000).
97. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR: Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478 (2009).
98. Champagne FA: Epigenetic mechanisms and the transgenerational effects of maternal care. Front. Neuroendocrinol. 29, 386-397 (2008).
99. Grewal SIS, Klar AJS: Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 86, 95-101 (1996).
100. Morgan HD, Sutherland HG, Martin DI, Whitelaw E: Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 23, 314-318 (1999).
101. Margueron RL, Reinberg D: Chromatin structure and the inheritance of epigenetic information. Nat. Rev. Genet. 11, 285-296 (2010).
102. Kaufman PD, Rando OJ: Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol. 22, 284-290 (2010).
103. Buchan JR, Parker R: Eukaryotic stress granules: the ins and outs of translation. Mol. Cell. 36, 932-941 (2009).
104. Anderson P, Kedersha N: RNA granules. J. Cell Biol. 172, 803-808 (2006).
105. Anderson P, Kedersha N: RNA granules: post-transcriptional and epigenetic modulators of gene expression. Nat. Rev. Mol. Cell Biol. 10, 430-436 (2009).
106. Kedersha N, Chen S, Gilks N et al.: Evidence that ternary complex (eIF2-GTP-tRNAiMet)-deficient preinitiation complexes are core constituents of mammalian stress granules. Mol. Biol. Cell. 13, 195-210 (2002).
107. Kedersha NL, Gupta M, Li W et al.: RNA-binding proteins Tia-1 and Tiar link the phosphorylation of Eif2 to the assembly of mammalian stress granules. J. Cell Biol. 147, 1431-1442 (1999).
108. Slanchev K, Stebler J, Goudarzi et al.: Control of dead end localization and activity - implications for the function of the protein in antagonizing miRNA function. Mech. Dev. 126, 270-277 (2009).