Novel insights into the genetic and epigenetic paternal contribution to the human embryo

Clinics

Volumn 68, Issue SUPPL. 1, 2013, Pages 5-14

  Kumar, Manoj ^a   Kumar, Kishlay ^a   Jain, Shalu ^a   Hassan, Tarannum ^a   Dada, Rima ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

DNA damage; DNA integrity; Epigenome; Messenger RNA (mRNA); Telomere

Indexed keywords

MICRORNA; RNA;

CHROMATIN; EMBRYO DEVELOPMENT; EPIGENETICS; FEMALE; FERTILIZATION; GENETICS; HUMAN; MALE; OOCYTE; PHYSIOLOGY; REVIEW; SPERMATOZOON;

CHROMATIN; EMBRYONIC DEVELOPMENT; EPIGENOMICS; FEMALE; FERTILIZATION; HUMANS; MALE; MICRORNAS; OOCYTES; RNA; SPERMATOZOA;

EID: 84875123218     PISSN: 18075932     EISSN: None     Source Type: Journal    
DOI: 10.6061/clinics/2013(Sup01)02     Document Type: Review

References (126)

1. Krawetz SA. Paternal contribution: new insights and future challenges. Nat Rev Genet. 2005;6(8):633-42, http://dx.doi.org/10.1038/nrg1654.
2. Carrell DT. Contributions of spermatozoa to embryogenesis: assays to evaluate their genetic and epigenetic fitness. Reprod Biomed Online. 2008;16(4):474-84, http://dx.doi.org/10.1016/S1472-6483(10)60454-3.
3. Matzuk MM, Lamb DJ. The biology of infertility: research advances and clinical challenges. Nat Med. 2008;14(11):1197-213, http://dx.doi.org/10.1038/nm.f.1895.
4. Barroso G, Valdespin C, Vega E, Kershenovich R, Avila R, Avendano C, et al. Developmental sperm contributions: fertilization and beyond. Fertil Steril. 2009;92(3):835-48, http://dx.doi.org/10.1016/j.fertnstert. 2009.06.030.
5. Sutovsky P, Schatten G. Paternal contributions to the mammalian zygote: fertilization after sperm-egg fusion. Int Rev Cytol. 2000;195:1-65, http://dx.doi.org/10.1016/S0074-7696(08)62703-5.
6. Ostermeier GC, Goodrich RJ, Moldenhauer JS, Diamond MP, Krawetz SA. A suite of novel human spermatozoal RNAs. J Androl. 2005;26(1):70-4.
7. Jenkins TG, Carrell DT. The paternal epigenome and embryogenesis: poising mechanisms for development. Asian J Androl. 2011;13(1):76-80.
8. Ralt D, Goldenberg M, Fetterolf P, Thompson D, Dor J, Mashiach S, et al. Sperm attraction to a follicular factor(s) correlates with human egg fertilizability. Proc Natl Acad Sci U S A. 1991;88(7):2840-4, http://dx. doi.org/10.1073/pnas.88.7.2840.
9. Ward WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod. 2010;16(1):30-6, http://dx.doi.org/10.1093/molehr/gap080.
10. Kumar K, Deka D, Singh A, Mitra DK, Vanitha BR, Dada R. Predictive value of DNA integrity analysis in idiopathic recurrent pregnancy loss following spontaneous conception. J Assist Reprod Genet. 2012.
11. Cebesoy FB, Aydos K, Unlu C. Effect of sperm chromatin damage on fertilization ratio and embryo quality post-ICSI. Arch Androl. 2006;52(5):397-402, http://dx.doi.org/10.1080/01485010600666953.
12. D'Occhio MJ, Hengstberger KJ, Johnston SD. Biology of sperm chromatin structure and relationship to male fertility and embryonic survival. Anim Reprod Sci. 2007;101(1-2):1-17, http://dx.doi.org/10. 1016/j.anireprosci.2007.01.005.
13. Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005;322(1):33-41, http://dx.doi.org/10.1007/s00441-005-1097-5.
14. Janny L, Menezo YJ. Evidence for a strong paternal effect on human preimplantation embryo development and blastocyst formation. Mol Reprod Dev. 1994;38(1):36-42, http://dx.doi.org/10.1002/mrd. 1080380107.
15. Venkatesh S, Singh A, Shamsi MB, Thilagavathi J, Kumar R, Mitra DK, et al. Clinical significance of sperm DNA damage threshold value in the assessment of male infertility. Reprod Sci. 2011;18(10):1005-13, http://dx.doi.org/10.1177/1933719111401662.
16. Belokopytova IA, Kostyleva EI, Tomilin AN, Vorob'ev VI. Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin. Mol Reprod Dev. 1993;34(1):53-7, http://dx.doi.org/10.1002/mrd.1080340109.
17. Andrabi SM. Mammalian sperm chromatin structure and assessment of DNA fragmentation. J Assist Reprod Genet. 2007;24(12):561-9, http://dx.doi.org/10.1007/s10815-007-9177-y.
18. Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010;93(4):1027-36, http://dx.doi.org/10.1016/j.fertnstert.2009.10.046.
19. Barratt CL, Aitken RJ, Bjorndahl L, Carrell DT, de Boer P, Kvist U, et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications-a position report. Hum Reprod. 2010;25(4):824-38, http://dx.doi.org/10.1093/humrep/dep465.
20. Zini A, Meriano J, Kader K, Jarvi K, Laskin CA, Cadesky K. Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod. 2005;20(12):3476-80, http://dx.doi.org/10.1093/humrep/dei266.
21. Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, et al. Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod. 2006;21(11):2876-81, http://dx.doi.org/10.1093/humrep/del251.
22. Simon L, Brunborg G, Stevenson M, Lutton D, McManus J, Lewis SE. Clinical significance of sperm DNA damage in assisted reproduction outcome. Hum Reprod. 2010;25(7):1594-608, http://dx.doi.org/10. 1093/humrep/deq103.
23. Greco E, Romano S, Iacobelli M, Ferrero S, Baroni E, Minasi MG, et al. ICSI in cases of sperm DNA damage: beneficial effect of oral antioxidant treatment. Hum Reprod. 2005;20(9):2590-4, http://dx.doi. org/10.1093/humrep/dei091.
24. Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, et al. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod. 2001;16(9):1912-21, http://dx.doi.org/10. 1093/humrep/16.9.1912.
25. Suganuma R, Yanagimachi R, Meistrich ML. Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod. 2005;20(11):3101-8, http://dx.doi.org/10.1093/humrep/dei169.
26. Olsen AK, Duale N, Bjoras M, Larsen CT, Wiger R, Holme JA, et al. Limited repair of 8-hydroxy-7,8-dihydroguanine residues in human testicular cells. Nucleic Acids Res. 2003;31(4):1351-63, http://dx.doi. org/10.1093/nar/gkg216.
27. Ward MA, Ward WS. A model for the function of sperm DNA degradation. Reprod Fertil Dev. 2004;16(5):547-54, http://dx.doi.org/10.1071/RD03072.
28. Tesarik J, Mendoza C, Greco E. Paternal effects acting during the first cell cycle of human preimplantation development after ICSI. Hum Reprod. 2002;17(1):184-9, http://dx.doi.org/10.1093/humrep/17.1.184.
29. Tesarik J, Greco E, Mendoza C. Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod. 2004;19(3):611-5, http://dx.doi.org/10.1093/humrep/deh127.
30. Shimura T, Toyoshima M, Taga M, Shiraishi K, Uematsu N, Inoue M, et al. The novel surveillance mechanism of the Trp53-dependent sphase checkpoint ensures chromosome damage repair and preimplantation-stage development of mouse embryos fertilized with x-irradiated sperm. Radiat Res. 2002;158(6):735-42, http://dx.doi.org/10.1667/0033-7587(2002)158[0735:TNSMOT]2.0.CO;2.
31. Adiga SK, Toyoshima M, Shimura T, Takeda J, Uematsu N, Niwa O. Delayed and stage specific phosphorylation of H2AX during preimplantation development of gamma-irradiated mouse embryos. Reproduction. 2007;133(2):415-22, http://dx.doi.org/10.1530/REP-06-0048.
32. Menezo Y, Dale B, Cohen M. DNA damage and repair in human oocytes and embryos: a review. Zygote. 2010;18(4):357-65, http://dx. doi.org/10.1017/S0967199410000286.
33. Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22(1):174-9.
34. Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S, et al. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Human Reproduction. 2012.
35. Zini A, Boman JM, Belzile E, Ciampi A. Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod. 2008;23(12):2663-8, http://dx.doi.org/10.1093/humrep/den321.
36. Gineitis AA, Zalenskaya IA, Yau PM, Bradbury EM, Zalensky AO. Human sperm telomere-binding complex involves histone H2B and secures telomere membrane attachment. J Cell Biol. 2000;151(7):1591-8, http://dx.doi.org/10.1083/jcb.151.7.1591.
37. Churikov D, Siino J, Svetlova M, Zhang K, Gineitis A, Morton Bradbury E, et al. Novel human testis-specific histone H2B encoded by the interrupted gene on the X chromosome. Genomics. 2004;84(4):745-56, http://dx.doi.org/10.1016/j.ygeno.2004.06.001.
38. 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(7254):473-8.
39. Arpanahi A, Brinkworth M, Iles D, Krawetz SA, Paradowska A, Platts AE, et al. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Genome Res. 2009;19(8):1338-49, http://dx.doi.org/10. 1101/gr.094953.109.
40. 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(2):458-69, http://dx.doi.org/10.1016/j. ydbio.2006.06.051.
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, http://dx.doi.org/10. 1186/1471-213X-8-34.
42. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, Braat DD, et al. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev. 2005;122(9):1008-22, http://dx.doi.org/10.1016/j.mod.2005. 04.009.
43. Ajduk A, Yamauchi Y, Ward MA. Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biol Reprod. 2006;75(3):442-51, http://dx.doi.org/10.1095/biolreprod.106.053223.
44. Ward WS, Kimura Y, Yanagimachi R. An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biol Reprod. 1999;60(3):702-6, http://dx.doi. org/10.1095/biolreprod60.3.702.
45. Kramer JA, Krawetz SA. Nuclear matrix interactions within the sperm genome. J Biol Chem. 1996;271(20):11619-22.
46. Shaman JA, Yamauchi Y, Ward WS. The sperm nuclear matrix is required for paternal DNA replication. J Cell Biochem. 2007;102(3):680-8, http://dx.doi.org/10.1002/jcb.21321.
47. Yamauchi Y, Shaman JA, Boaz SM, Ward WS. Paternal pronuclear DNA degradation is functionally linked to DNA replication in mouse oocytes. Biol Reprod. 2007;77(3):407-15, http://dx.doi.org/10.1095/biolreprod. 107.061473.
48. Premkumar E, Bhargava PM. Transcription and translation in bovine spermatozoa. Nat New Biol. 1972;240(100):139-43.
49. MacLaughlin J, Terner C. Ribonucleic acid synthesis by spermatozoa from the rat and hamster. Biochem J. 1973;133(4):635-9.
50. Hecht NB, Williams JL. Synthesis of RNA by separated heads and tails from bovine spermatozoa. Biol Reprod. 1978;19(3):573-9, http://dx.doi. org/10.1095/biolreprod19.3.573.
51. Pessot CA, Brito M, Figueroa J, Concha, Yanez, II A, Burzio LO. Presence of RNA in the sperm nucleus. Biochem Biophys Res Commun. 1989;158(1):272-8, http://dx.doi.org/10.1016/S0006-291X(89)80208-6.
52. Brewer L, Corzett M, Balhorn R. Condensation of DNA by spermatid basic nuclear proteins. J Biol Chem. 2002;277(41):38895-900, http://dx. doi.org/10.1074/jbc.M204755200.
53. Balhorn R. The protamine family of sperm nuclear proteins. Genome Biol. 2007;8(9):227, http://dx.doi.org/10.1186/gb-2007-8-9-227.
54. de la Fuente R, Parra MT, Viera A, Calvente A, Gomez R, Suja JA, et al. Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein. PLoS Genet. 2007;3(11):e198, http://dx.doi.org/10.1371/journal.pgen.0030198.
55. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell. 2003;4(4):497-508, http://dx.doi.org/10.1016/S1534-5807(03)00093-5.
56. Grunewald S, Paasch U, Glander HJ, Anderegg U. Mature human spermatozoa do not transcribe novel RNA. Andrologia. 2005;37(2-3):69-71, http://dx.doi.org/10.1111/j.1439-0272.2005.00656.x.
57. Kumar G, Patel D, Naz RK. c-MYC mRNA is present in human sperm cells. Cell Mol Biol Res. 1993;39(2):111-7.
58. Chiang MH, Steuerwald N, Lambert H, Main EK, Steinleitner A. Detection of human leukocyte antigen class I messenger ribonucleic acid transcripts in human spermatozoa via reverse transcriptionpolymerase chain reaction. Fertil Steril. 1994;61(2):276-80.
59. Rohwedder A, Liedigk O, Schaller J, Glander HJ, Werchau H. Detection of mRNA transcripts of beta 1 integrins in ejaculated human spermatozoa by nested reverse transcription-polymerase chain reaction. Mol Hum Reprod. 1996;2(7):499-505, http://dx.doi.org/10.1093/molehr/2.7.499.
60. Richter W, Dettmer D, Glander H. Detection of mRNA transcripts of cyclic nucleotide phosphodiesterase subtypes in ejaculated human spermatozoa. Mol Hum Reprod. 1999;5(8):732-6, http://dx.doi.org/10. 1093/molehr/5.8.732.
61. Goodwin LO, Karabinus DS, Pergolizzi RG, Benoff S. L-type voltagedependent calcium channel alpha-1C subunit mRNA is present in ejaculated human spermatozoa. Mol Hum Reprod. 2000;6(2):127-36, http://dx.doi.org/10.1093/molehr/6.2.127.
62. Goodwin LO, Karabinus DS, Pergolizzi RG. Presence of N-cadherin transcripts in mature spermatozoa. Mol Hum Reprod. 2000;6(6):487-97, http://dx.doi.org/10.1093/molehr/6.6.487.
63. Sachdeva G, Shah CA, Kholkute SD, Puri CP. Detection of progesterone receptor transcript in human spermatozoa. Biol Reprod. 2000;62(6):1610-4, http://dx.doi.org/10.1095/biolreprod62.6.1610.
64. Aquila S, Sisci D, Gentile M, Middea E, Catalano S, Carpino A, et al. Estrogen receptor (ER)alpha and ER beta are both expressed in human ejaculated spermatozoa: evidence of their direct interaction with phosphatidylinositol-3-OH kinase/Akt pathway. J Clin Endocrinol Metab. 2004;89(3):1443-51, http://dx.doi.org/10.1210/jc.2003-031681.
65. Lambard S, Galeraud-Denis I, Martin G, Levy R, Chocat A, Carreau S. Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: relationship to sperm motility and capacitation. Mol Hum Reprod. 2004;10(7):535-41, http://dx.doi.org/10.1093/molehr/gah064.
66. Aquila S, Gentile M, Middea E, Catalano S, Ando S. Autocrine regulation of insulin secretion in human ejaculated spermatozoa. Endocrinology. 2005;146(2):552-7.
67. Dadoune JP, Pawlak A, Alfonsi MF, Siffroi JP. Identification of transcripts by macroarrays, RT-PCR and in situ hybridization in human ejaculate spermatozoa. Mol Hum Reprod. 2005;11(2):133-40, http://dx. doi.org/10.1093/molehr/gah137.
68. Gilbert I, Bissonnette N, Boissonneault G, Vallee M, Robert C. A molecular analysis of the population of mRNA in bovine spermatozoa. Reproduction. 2007;133(6):1073-86, http://dx.doi.org/10.1530/REP-06-0292.
69. Bissonnette N, Levesque-Sergerie JP, Thibault C, Boissonneault G. Spermatozoal transcriptome profiling for bull sperm motility: a potential tool to evaluate semen quality. Reproduction. 2009;138(1):65-80, http://dx.doi.org/10.1530/REP-08-0503.
70. Boerke A, Dieleman SJ, Gadella BM. A possible role for sperm RNA in early embryo development. Theriogenology. 2007;68 Suppl 1:S147-55, http://dx.doi.org/10.1016/j.theriogenology.2007.05.058.
71. Miller D, Briggs D, Snowden H, Hamlington J, Rollinson S, Lilford R, et al. A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis. Gene. 1999;237(2):385-92, http://dx.doi.org/10.1016/S0378-1119(99)00324-8.
72. Lavitrano M, Busnelli M, Cerrito MG, Giovannoni R, Manzini S, Vargiolu A. Sperm-mediated gene transfer. Reprod Fertil Dev. 2006;18(1-2):19-23, http://dx.doi.org/10.1071/RD05124.
73. Smith K, Spadafora C. Sperm-mediated gene transfer: applications and implications. Bioessays. 2005;27(5):551-62, http://dx.doi.org/10.1002/bies.20211.
74. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature. 2004;429(6988):154, http://dx.doi.org/10.1038/429154a.
75. Rassoulzadegan M, Grandjean V, Gounon P, Vincent S, Gillot I, Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature. 2006;441(7092):469-74, http://dx.doi.org/10.1038/nature04674.
76. Wagner KD, Wagner N, Ghanbarian H, Grandjean V, Gounon P, Cuzin F, et al. RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell. 2008;14(6):962-9, http://dx.doi. org/10.1016/j.devcel.2008.03.009.
77. Gur Y, Breitbart H. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 2006;20(4):411-6, http://dx.doi.org/10.1101/gad.367606.
78. Liu WM, Pang RT, Chiu PC, Wong BP, Lao K, Lee KF, et al. Spermborne microRNA-34c is required for the first cleavage division in mouse. Proc Natl Acad Sci U S A. 2012;109(2):490-4, http://dx.doi.org/10.1073/pnas.1110368109.
79. Krawetz SA, Kruger A, Lalancette C, Tagett R, Anton E, Draghici S, et al. A survey of small RNAs in human sperm. Hum Reprod. 2011;26(12):3401-12, http://dx.doi.org/10.1093/humrep/der329.
80. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 2006;20(13):1732-43, http://dx.doi.org/10.1101/gad.1425706.
81. Luo L, Ye L, Liu G, Shao G, Zheng R, Ren Z, et al. Microarray-based approach identifies differentially expressed microRNAs in porcine sexually immature and mature testes. PLoS One. 2010;5(8):e11744, http://dx.doi.org/10.1371/journal.pone.0011744.
82. Platts AE, Dix DJ, Chemes HE, Thompson KE, Goodrich R, Rockett JC, et al. Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet. 2007;16(7):763-73, http://dx. doi.org/10.1093/hmg/ddm012.
83. Wang H, Zhou Z, Xu M, Li J, Xiao J, Xu ZY, et al. A spermatogenesisrelated gene expression profile in human spermatozoa and its potential clinical applications. J Mol Med. 2004;82(5):317-24, http://dx.doi.org/10.1007/s00109-004-0526-3.
84. Ostermeier GC, Dix DJ, Miller D, Khatri P, Krawetz SA. Spermatozoal RNA profiles of normal fertile men. Lancet. 2002;360(9335):772-7, http://dx.doi.org/10.1016/S0140-6736(02)09899-9.
85. Zhao Y, Li Q, Yao C, Wang Z, Zhou Y, Wang Y, et al. Characterization and quantification of mRNA transcripts in ejaculated spermatozoa of fertile men by serial analysis of gene expression. Hum Reprod. 2006;21(6):1583-90, http://dx.doi.org/10.1093/humrep/del027.
86. Garcia-Herrero S, Garrido N, Martinez-Conejero JA, Remohi J, Pellicer A, Meseguer M. Differential transcriptomic profile in spermatozoa achieving pregnancy or not via ICSI. Reprod Biomed Online. 2011;22(1):25-36, http://dx.doi.org/10.1016/j.rbmo.2010.09.013.
87. Kocabas AM, Crosby J, Ross PJ, Otu HH, Beyhan Z, Can H, et al. The transcriptome of human oocytes. Proc Natl Acad Sci U S A. 2006;103(38):14027-32, http://dx.doi.org/10.1073/pnas.0603227103.
88. Avendano C, Franchi A, Jones E, Oehninger S. Pregnancy-specific {beta}-1-glycoprotein 1 and human leukocyte antigen-E mRNA in human sperm: differential expression in fertile and infertile men and evidence of a possible functional role during early development. Hum Reprod. 2009;24(2):270-7, http://dx.doi.org/10.1093/humrep/den381.
89. Motran CC, Diaz FL, Gruppi A, Slavin D, Chatton B, Bocco JL. Human pregnancy-specific glycoprotein 1a (PSG1a) induces alternative activation in human and mouse monocytes and suppresses the accessory celldependent T cell proliferation. J Leukoc Biol. 2002;72(3):512-21.
90. Meseguer M, de los Santos MJ, Simon C, Pellicer A, Remohi J, Garrido N. Effect of sperm glutathione peroxidases 1 and 4 on embryo asymmetry and blastocyst quality in oocyte donation cycles. Fertil Steril. 2006;86(5):1376-85, http://dx.doi.org/10.1016/j.fertnstert.2006. 03.053.
91. Carrell DT, Liu L. Altered protamine 2 expression is uncommon in donors of known fertility, but common among men with poor fertilizing capacity, and may reflect other abnormalities of spermiogenesis. J Androl. 2001;22(4):604-10.
92. Cho C, Jung-Ha H, Willis WD, Goulding EH, Stein P, Xu Z, et al. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod. 2003;69(1):211-7, http://dx.doi.org/10.1095/biolreprod.102.015115.
93. Zalenskaya IA, Bradbury EM, Zalensky AO. Chromatin structure of telomere domain in human sperm. Biochem Biophys Res Commun. 2000;279(1):213-8, http://dx.doi.org/10.1006/bbrc.2000.3917.
94. Rodriguez S, Goyanes V, Segrelles E, Blasco M, Gosalvez J, Fernandez JL. Critically short telomeres are associated with sperm DNA fragmentation. Fertil Steril. 2005;84(4):843-5, http://dx.doi.org/10. 1016/j.fertnstert.2005.05.014.
95. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008;9(2):129-40, http://dx.doi.org/10.1038/nrg2295.
96. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293(5532):1089-93, http://dx.doi.org/10. 1126/science.1063443.
97. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol. 2005;278(2):440-58, http://dx.doi.org/10.1016/j.ydbio. 2004.11.025.
98. Ward WS, Coffey DS. DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod. 1991;44(4):569-74, http://dx.doi.org/10.1095/biolreprod44.4.569.
99. El Hajj N, Zechner U, Schneider E, Tresch A, Gromoll J, Hahn T, et al. Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev. 2011;5(2):60-9, http://dx.doi.org/10.1159/000323806.
100. Nanassy L, Carrell DT. Abnormal methylation of the promoter of CREM is broadly associated with male factor infertility and poor sperm quality but is improved in sperm selected by density gradient centrifugation. Fertil Steril. 2011;95(7):2310-4, http://dx.doi.org/10. 1016/j.fertnstert.2011.03.096.
101. Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, et al. Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod. 2010;25(10):2647-54, http://dx.doi.org/10.1093/humrep/deq200.
102. Pacheco SE, Houseman EA, Christensen BC, Marsit CJ, Kelsey KT, Sigman M, et al. Integrative DNA methylation and gene expression analyses identify DNA packaging and epigenetic regulatory genes associated with low motility sperm. PLoS One. 2011;6(6):e20280, http://dx.doi.org/10.1371/journal.pone.0020280.
103. Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 2011;25(7):679-84, http://dx.doi.org/10.1101/gad.2036011.
104. Ebstein RP, Israel S, Chew SH, Zhong S, Knafo A. Genetics of human social behavior. Neuron. 2010;65(6):831-44, http://dx.doi.org/10.1016/j.neuron.2010.02.020.
105. Torgersen S. The nature (and nurture) of personality disorders. Scand J Psychol. 2009;50(6):624-32.
106. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature. 2011;473(7347):394-7, http://dx.doi.org/10.1038/nature10102.
107. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS. Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell. 2006;10(4):521-9, http://dx.doi.org/10.1016/j.devcel.2006.02.009.
108. Namekawa SH, Park PJ, Zhang LF, Shima JE, McCarrey JR, Griswold MD, et al. Postmeiotic sex chromatin in the male germline of mice. Curr Biol. 2006;16(7):660-7, http://dx.doi.org/10.1016/j.cub.2006.01.066.
109. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. Establishment of male-specific epigenetic information. Gene. 2005;345(2):139-53, http://dx.doi.org/10.1016/j.gene.2004.12.004.
110. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A. 2007;104(1):228-33, http://dx.doi.org/10. 1073/pnas.0607521104.
111. Hayashi K, Yoshida K, Matsui Y. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature. 2005;438(7066):374-8, http://dx.doi.org/10.1038/nature04112.
112. Hata K, Okano M, Lei H, Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development. 2002;129(8):1983-93.
113. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science. 2001; 294(5551):2536-9, http://dx.doi.org/10.1126/science.1065848.
114. Marques CJ, Carvalho F, Sousa M, Barros A. Genomic imprinting in disruptive spermatogenesis. Lancet. 2004;363(9422):1700-2, http://dx. doi.org/10.1016/S0140-6736(04)16256-9.
115. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 2007;16(21):2542-51, http://dx.doi. org/10.1093/hmg/ddm187.
116. Horsthemke B, Wagstaff J. Mechanisms of imprinting of the Prader-Willi/Angelman region. Am J Med Genet A. 2008;146A(16):2041-52.
117. Benchaib M, Ajina M, Lornage J, Niveleau A, Durand P, Guerin JF. Quantitation by image analysis of global DNA methylation in human spermatozoa and its prognostic value in in vitro fertilization: a preliminary study. Fertil Steril. 2003;80(4):947-53, http://dx.doi.org/10.1016/S0015-0282(03)01151-8.
118. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A, et al. Influence of global sperm DNA methylation on IVF results. Hum Reprod. 2005;20(3):768-73, http://dx.doi.org/10.1093/humrep/deh684.
119. Murphy SK, Jirtle RL. Imprinting evolution and the price of silence. Bioessays. 2003;25(6):577-88, http://dx.doi.org/10.1002/bies.10277.
120. Weaver JR, Susiarjo M, Bartolomei MS. Imprinting and epigenetic changes in the early embryo. Mamm Genome. 2009;20(9-10):532-43, http://dx.doi.org/10.1007/s00335-009-9225-2.
121. Mathers JC, McKay JA. Epigenetics-potential contribution to fetal programming. Adv Exp Med Biol. 2009;646:119-23, http://dx.doi.org/10.1007/978-1-4020-9173-5_13.
122. Ruden DM, Lu X. Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila. Curr Genomics. 2008;9(7):500-8, http://dx.doi.org/10.2174/138920208786241207.
123. Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLoS Genet. 2006;2(4):e49, http://dx.doi.org/10.1371/journal.pgen.0020049.
124. Waterland RA, Travisano M, Tahiliani KG. Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J. 2007;21(12):3380-5, http://dx.doi.org/10. 1096/fj.07-8229com.
125. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132(8 Suppl):2393S-400S.
126. Martin LA, Davies GL, Weigel MT, Betambeau N, Hills MJ, Salter J, et al. Pre-surgical study of the biological effects of the selective cyclooxygenase-2 inhibitor celecoxib in patients with primary breast cancer. Breast Cancer Res Treat. 2010;123(3):829-36, http://dx.doi.org/10.1007/s10549-010-1100-z.