Environment-sensitive epigenetics and the heritability of complex diseases

Genetics

Volumn 189, Issue 4, 2011, Pages 1377-1387

  Furrow, Robert E ^a,b   Christiansen, Freddy B ^b   Feldman, Marcus W ^a  

^a STANFORD UNIVERSITY   (United States)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ARTICLE; DNA MODIFICATION; EPIGENETICS; GENETIC DISORDER; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE ENVIRONMENT INTERACTION; HEREDITY; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTION;

EID: 83455243198     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.111.131912     Document Type: Article

References (77)

1. Abdolmaleky, H. M., S. Thiagalingam, and M. Wilcox, 2005 Genetics and epigenetics in major psychiatric disorders: dilemmas, achievements, applications, and future scope. Am. J. Pharmacogenomics 5: 149-160.
2. Bird, A., 2007 Perceptions of epigenetics. Nature 447: 396-398.
3. Bonduriansky, R., and T. Day, 2009 Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40: 103-125.
4. Bossdorf, O., C. Richards, and M. Pigliucci, 2008 Epigenetics for ecologists. Ecol. Lett. 11: 106-115.
5. Cavalli-Sforza, L., and M. Feldman, 1973 Cultural vs. biological inheritance: phenotypic transmission from parents to children (a theory of the effect of parental phenotypes on children's phenotypes). Am. J. Hum. Genet. 25: 618-637.
6. Cavalli-Sforza, L., and M. Feldman, 1981 Cultural Transmission and Evolution: A Quantitative Approach. Princeton University Press, Princeton, NJ.
7. Cervera, M. T., L. Ruiz-García, and J. M. Martínez-Zapater, 2002 Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive aflp markers. Mol. Genet. Genomics 268: 543-552.
8. Cooney, C. A., A. A. Dave, and G. L. Wolff, 2002 Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J. Nutr. 132: 2393S-2400S.
9. Cropley, J. E., C. M. Suter, K. B. Beckman, and D. I. K. Martin, 2006 Germ-line epigenetic modification of the murine a vy allele by nutritional supplementation. Proc. Natl. Acad. Sci. USA 103: 17308-17312.
10. Cubas, P., C. Vincent, and E. Coen, 1999 An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401: 157-161.
11. Danchin, E., and R. Wagner, 2010 Inclusive heritability: combining genetic and non-genetic information to study animal behavior and culture. Oikos 119: 210-218.
12. Danchin, E., A. Charmantier, F. A. Champagne, A. Mesoudi, B. Pujol et al., 2011 Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat. Rev. Genet. 12: 475-486.
13. Day, T., and R. Bonduriansky, 2011 A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 178: E18-E36.
14. Egger, G., G. Liang, A. Aparicio, and P. Jones, 2004 Epigenetics in human disease and prospects for epigenetic therapy. Nature 429: 457-463.
15. Eichler, E., J. Flint, G. Gibson, A. Kong, S. Leal et al., 2010 VIEWPOINT Missing heritability and strategies for finding the underlying causes of complex disease. Nat. Rev. Genet. 11: 446-450.
16. Elango, N., B. G. Hunt, M. A. D. Goodisman, and S. V. Yi, 2009 DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl. Acad. Sci. USA 106: 11206-11211.
17. Falconer, D., and T. Mackay, 1996 Introduction to Quantitative Genetics. Longman, New York.
18. Feinberg, A. P., 2007 Phenotypic plasticity and the epigenetics of human disease. Nature 447: 433-440.
19. Feldman, M., and L. Cavalli-Sforza, 1979 Aspects of variance and covariance analysis with cultural inheritance. Theor. Popul. Biol. 15: 276-307.
20. Feldman, M., and R. Lewontin, 1975 The heritability hang-up. Science 190: 1163-1168.
21. Feldman, M., F. Christiansen, and S. Otto, 1995 Statistics of Discrete-Valued Traits Under Vertical Transmission. Working paper no. 65, Morrison Institute for Population Studies, Stanford University, Stanford, CA. Available at: http://hsblogs.stanford.edu/morrison/files/2011/02/65.pdf.
22. Feldman, M., S. Otto, and F. Christiansen, 2000 Genes, culture, and inequality, pp. 61-85 in Meritocracy and Economic Inequality, edited by K. Arrow, S. Bowles, and S. Durlauf. Princeton University Press, Princeton, NJ.
23. Gaál, B., J. W. Pitchford, and A. J. Wood, 2010 Exact results for the evolution of stochastic switching in variable asymmetric environments. Genetics 184: 1113-1119.
24. Gajdusek, D., C. Gibbs, and M. Alpers, 1966 Experimental transmission of a Kuru-like syndrome to chimpanzees. Nature 209:794.
25. Goldstein, D., 2009 Common genetic variation and human traits. N. Engl. J. Med. 360: 1696-1698.
26. Harper, P. S., 1977 Mendelian inheritance or transmissible agent? The lesson Kuru and the Australia antigen. J. Med. Genet. 14: 389-398.
27. Heijmans, B. T., E. W. Tobi, A. D. Stein, H. Putter, G. J. Blauw et al., 2008 Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci. USA 105: 17046-17049.
28. Henderson, I. R., and S. E. Jacobsen, 2007 Epigenetic inheritance in plants. Nature 447: 418-424.
29. Herrera, C. M., and P. Bazaga, 2011 Untangling individual variation in natural populations: ecological, genetic and epigenetic correlates of long-term inequality in herbivory. Mol. Ecol. 20: 1675-1688.
30. Hirst, M., and M. A. Marra, 2009 Epigenetics and human disease. Int. J. Biochem. Cell Biol. 41: 136-146.
31. Jablonka, E., and M. J. Lamb, 1989 The inheritance of acquired epigenetic variations. J. Theor. Biol. 139: 69-83.
32. Jablonka, E., and G. Raz, 2009 Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q. Rev. Biol. 84: 131-176.
33. Jiang, Y.-H., J. Bressler, and A. L. Beaudet, 2004 Epigenetics and human disease. Annu. Rev. Genomics Hum. Genet. 5: 479-510.
34. Jirtle, R., and M. Skinner, 2007 Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8: 253-262.
35. Kamin, L., and A. Goldberger, 2002 Twin studies in behavioral research: a skeptical view. Theor. Popul. Biol. 61: 83-95.
36. Katari, S., N. Turan, M. Bibikova, O. Erinle, R. Chalian et al., 2009 DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum. Mol. Genet. 18: 3769-3778.
37. Keyte, A. L., R. Percifield, B. Liu, and J. F. Wendel, 2006 Intraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum l.). J. Hered. 97: 444-450.
38. King, O. D., and J. Masel, 2007 The evolution of bet-hedging adaptations to rare scenarios. Theor. Popul. Biol. 72: 560-575.
39. Kucharski, R., J. Maleszka, S. Foret, and R. Maleszka, 2008 Nutritional control of reproductive status in honeybees via DNA methylation. Science 319: 1827-1830.
40. Kussell, E., and S. Leibler, 2005 Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078.
41. Lachmann, M., and E. Jablonka, 1996 The inheritance of phenotypes: an adaptation to fluctuating environments. J. Theor. Biol. 181: 1-9.
42. Layzer, D., 1974 Heritability analyses of IQ scores-science or numerology. Science 183: 1259-1266.
43. Liberman, U., J. Van Cleve, and M. W. Feldman, 2011 On the evolution of mutation in changing environments: recombination and phenotypic switching. Genetics 187: 837-851.
44. Lillycrop, K. A., J. L. Slater-Jefferies, M. A. Hanson, K. M. Godfrey, A. A. Jackson et al., 2007 Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br. J. Nutr. 97: 1064-1073.
45. Lindenbaum, S., 2008 Understanding Kuru: the contribution of anthropology and medicine. Philos. Trans. R. Soc. B Biol. Sci. 363: 3715-3720.
46. Lyko, F., S. Foret, R. Kucharski, S. Wolf, C. Falckenhayn et al., 2010 The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol. 8: e1000506.
47. Maher, B., 2008 Personal genomes: the case of the missing heritability. Nature 456: 18-21.
48. Martienssen, R. A., and V. Colot, 2001 DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293: 1070-1074.
49. Meaney, M. J., and M. Szyf, 2005 Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci. 7: 103-123.
50. Moran, P., 1973 A note on heritability and correlation between relatives. Ann. Hum. Genet. 37: 217.
51. Otto, S., M. Feldman, and F. Christiansen, 1995 Genetics and Cultural Inheritance of Continuous Traits. Working paper no. 64, Morrison Institute for Population Studies, Stanford University, Stanford, CA. Available at: http://hsblogs.stanford.edu/morrison/files/2011/02/64.pdf.
52. Petronis, A., 2010 Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature 465: 721-727.
53. Rakyan, V., and S. Beck, 2006 Epigenetic variation and inheritance in mammals. Curr. Opin. Genet. Dev. 16: 573-577.
54. Rakyan, V. K., J. Preis, H. D. Morgan, and E. Whitelaw, 2001 The marks, mechanisms and memory of epigenetic states in mammals. Biochem. J. 356: 1-10.
55. Riddle, N. C., and E. J. Richards, 2002 The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162: 355-363.
56. Rutten, B. P. F., and J. Mill, 2009 Epigenetic mediation of environmental influences in major psychotic disorders. Schizophr. Bull. 35: 1045-1056.
57. Salathe, M., J. Van Cleve, and M. W. Feldman, 2009 Evolution of stochastic switching rates in asymmetric fitness landscapes. Genetics 182: 1159-1164.
58. Sandovici, I., N. H. Smith, M. D. Nitert, M. Ackers-Johnson, S. Uribe-Lewis et al., 2011 Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the hnf4a gene in rat pancreatic islets. Proc. Natl. Acad. Sci. USA 108: 5449-5454.
59. Shindo, C., C. Lister, P. Crevillen, M. Nordborg, and C. Dean, 2006 Variation in the epigenetic silencing of flc contributes to natural variation in Arabidopsis vernalization response. Genes Dev. 20: 3079-3083.
60. Slatkin, M., 2009 Epigenetic inheritance and the missing heritability problem. Genetics 182: 845-850.
61. St. Clair, D., M. Xu, P. Wang, Y. Yu, Y. Fang et al., 2005 Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 294: 557-562.
62. Susser, E. S., and S. P. Lin, 1992 Schizophrenia after prenatal exposure to the Dutch hunger winter of 1944-1945. Arch. Gen. Psychiatry 49: 983-988.
63. Susser, E. S., R. Neugebauer, H. Hoek, A. Brown, S. Lin et al., 1996 Schizophrenia after prenatal famine-further evidence. Arch. Gen. Psychiatry 53: 25-31.
64. Tal, O., E. Kisdi, and E. Jablonka, 2010 Epigenetic contribution to covariance between relatives. Genetics 184: 1037-1050.
65. Tsankova, N., W. Renthal, A. Kumar, and E. J. Nestler, 2007 Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 8: 355-367.
66. Vaughn, M. W., M. Tanurdzić, Z. Lippman, H. Jiang, R. Carrasquillo et al., 2007 Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol. 5: e174.
67. Verhoeven, K. J. F., J. J. Jansen, P. J. van Dijk, and A. Biere, 2010 Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 185: 1108-1118.
68. Waddington, C., 1957 The Strategy of the Genes. Allen & Unwin, London.
69. Waterland, R., and R. Jirtle, 2003 Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell. Biol. 23: 5293-5300.
70. Waterland, R. A., and R. L. Jirtle, 2004 Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20: 63-68.
71. Waterland, R. A., D. C. Dolinoy, J.-R. Lin, C. A. Smith, X. Shi et al., 2006 Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 44: 401-406.
72. Waterland, R. A., R. Kellermayer, E. Laritsky, P. Rayco-Solon, R. A. Harris et al., 2010 Season of conception in rural Gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet. 6: e1001252.
73. Weaver, I. C. G., 2007 Epigenetic programming by maternal behavior and pharmacological intervention. Nature vs. nurture: let's call the whole thing off. Epigenetics 2: 22-28.
74. Weaver, I., N. Cervoni, F. Champagne, A. D'Alessio, S. Sharma et al., 2004 Epigenetic programming by maternal behavior. Nat. Neurosci. 7: 847-854.
75. Weaver, I. C. G., M. J. Meaney, and M. Szyf, 2006 Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. USA 103: 3480-3485.
76. Wolf, D. M., V. V. Vazirani, and A. P. Arkin, 2005 Diversity in times of adversity: probabilistic strategies in microbial survival games. J. Theor. Biol. 234: 227-253.
77. Wolff, G. L., R. L. Kodell, S. R. Moore, and C. A. Cooney, 1998 Maternal epigenetics and methyl supplements affect agouti gene expression in avy/a mice. FASEB J. 12: 949-957.