The paternal hidden agenda: Epigenetic inheritance through sperm chromatin

Epigenetics

Volumn 5, Issue 5, 2010, Pages

  Puri, Deepika ^a   Dhawan, Jyotsna ^a,b   Mishra, Rakesh K ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Epigenetic inheritance; Genome environment interaction; Histone modifications; Maternal effect; Parental conflict; Sperm chromatin; Spermeiogenesis

Indexed keywords

HISTONE; PROTAMINE;

ACETYLATION; ARTICLE; BIOINFORMATICS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DISEASE PREDISPOSITION; DNA METHYLATION; EMBRYO DEVELOPMENT; ENVIRONMENT; ENVIRONMENTAL FACTOR; EPIGENETICS; FERTILIZATION; GENE LOCUS; HEREDITY; HETEROCHROMATIN; HUMAN; INHERITANCE; LIFESTYLE; NONHUMAN; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SPERM; SPERMATOGENESIS; UBIQUITINATION; ZYGOTE;

EUKARYOTA;

EID: 77954664328     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.5.5.12005     Document Type: Article

References (68)

1. Bonduriansky RDT. Nongenetic Inheritance and Its Evolutionary Implications. Annu Rev Ecol Evol Syst 2009; 40:22.
2. Takeda S, Paszkowski J. DNA methylation and epigenetic inheritance during plant gametogenesis. Chromosoma 2006; 115:27-35.
3. Pembrey ME. Time to take epigenetic inheritance seriously. Eur J Hum Genet 2002; 10:669-71.
4. Whitelaw NC, Whitelaw E. How lifetimes shape epigenotype within and across generations. Hum Mol Genet 2006; 15:131-7.
5. Henikoff S, Furuyama T, Ahmad K. Histone variants, nucleosome assembly and epigenetic inheritance. Trends Genet 2004; 20:320-6.
6. Kornberg RD. Chromatin structure: a repeating unit of histones and DNA. Science 1974; 184:868-71.
7. Latham KE. Epigenetic modification and imprinting of the mammalian genome during development. Curr Top Dev Biol 1999; 43:1-49.
8. Cavalli G. Chromatin and epigenetics in development: blending cellular memory with cell fate plasticity. Development 2006; 133:2089-94.
9. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 2002; 3:662-73.
10. Probst AV, Dunleavy E, Almouzni G. Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 2009; 10:192-206.
11. Chong S, Whitelaw E. Epigenetic germline inheritance. Curr Opin Genet Dev 2004; 14:692-6.
12. Chandler VL, Stam M. Chromatin conversations: mechanisms and implications of paramutation. Nat Rev Genet 2004; 5:532-44.
13. Brink RA. Paramutation at the R locus in maize. Cold Spring Harb Symp Quant Biol 1958; 23:379-91.
14. Brink RA. A Genetic Change Associated with the R Locus in Maize Which Is Directed and Potentially Reversible. Genetics 1956; 41:872-89.
15. Mittelsten Scheid O, Afsar K, Paszkowski J. Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana. Nat Genet 2003; 34:450-4.
16. Cubas P, Vincent C, Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 1999; 401:157-61.
17. Grewal SI, Klar AJ. Chromosomal inheritance of epigenetic states in fission yeast during mitosis and meiosis. Cell 1996; 86:95-101.
18. Grewal SI, Elgin SC. Heterochromatin: new possibilities for the inheritance of structure. Curr Opin Genet Dev 2002; 12:178-87.
19. Thon G, Cohen A, Klar AJ. Three additional linkage groups that repress transcription and meiotic recombination in the mating-type region of Schizosaccharomyces pombe. Genetics 1994; 138:29-38.
20. Grewal SI, Bonaduce MJ, Klar AJ. Histone deacetylase homologs regulate epigenetic inheritance of transcriptional silencing and chromosome segregation in fission yeast. Genetics 1998; 150:563-76.
21. Cavalli G, Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell 1998; 93:505-18.
22. Rutherford SL, Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature 1998; 396:336-42.
23. Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, Ruden DM. Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nat Genet 2003; 33:70-4.
24. Sharma A, Singh P. Detection of transgenerational spermatogenic inheritance of adult male acquired CNS gene expression characteristics using a Drosophila systems model. PLoS One 2009; 4:5763.
25. Rakyan VK, Blewitt ME, Druker R, Preis JI, Whitelaw E. Metastable epialleles in mammals. Trends Genet 2002; 18:348-51.
26. Morgan HD, Sutherland HG, Martin DI, Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 1999; 23:314-8.
27. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 1998; 12:949-57.
28. Waterland RA. Do maternal methyl supplements in mice affect DNA methylation of offspring? J Nutr 2003; 133:238.
29. Buiting K, Gross S, Lich C, Gillessen-Kaesbach G, el-Maarri O, Horsthemke B. Epimutations in PraderWilli and Angelman syndromes: a molecular study of 136 patients with an imprinting defect. Am J Hum Genet 2003; 72:571-7.
30. Suter CM, Martin DI, Ward RL. Germline epimutation of MLH1 in individuals with multiple cancers. Nat Genet 2004; 36:497-501.
31. Whitelaw NC, Whitelaw E. Transgenerational epigenetic inheritance in health and disease. Curr Opin Genet Dev 2008; 18:273-9.
32. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, et al. Sex-specific, maleline transgenerational responses in humans. Eur J Hum Genet 2006; 14:159-66.
33. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature 2009; 460:473-8.
34. Ward WS, Coffey DS. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod 1991; 44:569-74.
35. Wykes SM, Krawetz SA. The structural organization of sperm chromatin. J Biol Chem 2003; 278:29471-7.
36. Kopecny V, Pavlok A. Autoradiographic study of mouse spermatozoan arginine-rich nuclear protein in fertilization. J Exp Zool 1975; 191:85-96.
37. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33:245-54.
38. Senthilkumar R, Mishra RK. Novel motifs distinguish multiple homologues of Polycomb in vertebrates: expansion and diversification of the epigenetic toolkit. BMC Genomics 2009; 10:549.
39. Bao S, Tang F, Li X, Hayashi K, Gillich A, Lao K, et al. Epigenetic reversion of post-implantation epiblast to pluripotent embryonic stem cells. Nature 2009; 461:1292-5.
40. Gatewood JM, Cook GR, Balhorn R, Schmid CW, Bradbury EM. Isolation of four core histones from human sperm chromatin representing a minor subset of somatic histones. J Biol Chem 1990; 265:20662-6.
41. van der Heijden GW, Ramos L, Baart EB, van den Berg IM, Derijck AA, van der Vlag J, et al. Sperm-derived histones contribute to zygotic chromatin in humans. BMC Dev Biol 2008; 8:34.
42. van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J, de Boer P. Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol 2006; 298:458-69.
43. Wu F, Caron C, De Robertis C, Khochbin S, Rousseaux S. Testis-specific histone variants H2AL1/2 rapidly disappear from paternal heterochromatin after fertilization. J Reprod Dev 2008; 54:413-7.
44. Gatewood JM, Cook GR, Balhorn R, Bradbury EM, Schmid CW. Sequence-specific packaging of DNA in human sperm chromatin. Science 1987; 236:962-4.
45. Gardiner-Garden M, Ballesteros M, Gordon M, Tam PP. Histone-and protamine-DNA association: conservation of different patterns within the betaglobin domain in human sperm. Mol Cell Biol 1998; 18:3350-6.
46. Ooi SL, Henikoff S. Germline histone dynamics and epigenetics. Curr Opin Cell Biol 2007; 19:257-65.
47. Carrell DT, Hammoud SS. The human sperm epigenome and its potential role in embryonic development. Mol Hum Reprod 16:37-47.
48. Monesi V. Ribonucleic Acid Synthesis during Mitosis and Meiosis in the Mouse Testis. J Cell Biol 1964; 22:521-32.
49. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315-26.
50. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM. Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature; 463:1042-7.
51. Okada Y, Yamagata K, Hong K, Wakayama T, Zhang Y. A role for the elongator complex in zygotic paternal genome demethylation. Nature 463:554-8.
52. Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S, Feil R. Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J 2007; 26:720-9.
53. Meistrich ML, Trostle-Weige PK, Lin R, Bhatnagar YM, Allis CD. Highly acetylated H4 is associated with histone displacement in rat spermatids. Mol Reprod Dev 1992; 31:170-81.
54. Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Sele B, et al. Regulated hyperacetylation of core histones during mouse spermatogenesis: involvement of histone deacetylases. Eur J Cell Biol 2000; 79:950-60.
55. Nair M, Nagamori I, Sun P, Mishra DP, Rheaume C, Li B, et al. Nuclear regulator Pygo2 controls spermiogenesis and histone H3 acetylation. Dev Biol 2008; 320:446-55.
56. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet 2007; 8:253-62.
57. Yajnik CS. Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J Nutr 2004; 134:205-10.
58. Talmud PJ. Gene-environment interaction and its impact on coronary heart disease risk. Nutr Metab Cardiovasc Dis 2007; 17:148-52.
59. Rutten BP, Mill J. Epigenetic mediation of environmental influences in major psychotic disorders. Schizophr Bull 2009; 35:1045-56.
60. Sharpe RM. Lifestyle and environmental contribution to male infertility. Br Med Bull 2000; 56:630-42.
61. Miller RL, Ho SM. Environmental epigenetics and asthma: current concepts and call for studies. Am J Respir Crit Care Med 2008; 177:567-73.
62. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry 1996; 53:25-31.
63. Susser E, Brown AS, Klonowski E, Allen RH, Lindenbaum J. Schizophrenia and impaired homocysteine metabolism: a possible association. Biol Psychiatry 1998; 44:141-3.
64. Wohl M, Gorwood P. Paternal ages below or above 35 years old are associated with a different risk of schizophrenia in the offspring. Eur Psychiatry 2007; 22:22-6.
65. Malaspina D, Harlap S, Fennig S, Heiman D, Nahon D, Feldman D, et al. Advancing paternal age and the risk of schizophrenia. Arch Gen Psychiatry 2001; 58:361-7.
66. Hayashi K, Surani MA. Resetting the epigenome beyond pluripotency in the germline. Cell Stem Cell 2009; 4:493-8.
67. Surani MA, Durcova-Hills G, Hajkova P, Hayashi K, Tee WW. Germ line, stem cells and epigenetic repro gramming. Cold Spring Harb Symp Quant Biol 2008; 73:9-15.
68. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22.