Epigenetic alterations in sperm associated with male infertility

Congenital Anomalies

Volumn 55, Issue 3, 2015, Pages 133-144

  Kitamura, Akane ^a   Miyauchi, Naoko ^a   Hamada, Hirotaka ^a   Hiura, Hitoshi ^a   Chiba, Hatsune ^a   Okae, Hiroaki ^a   Sato, Akiko ^a   John, Rosalind M ^b   Arima, Takahiro ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Assisted reproductive technologies; DNA methylation; Genomic imprinting; Genomic imprinting disorders; Male infertility

Indexed keywords

ENDOCRINE DISRUPTOR;

ASTHENOSPERMIA; DNA METHYLATION; DNA MODIFICATION; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE GENITAL TRACT INFECTION; FERTILIZATION; GAMETOGENESIS; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC VARIABILITY; GENOME IMPRINTING; GENOMIC IMPRINTING DISORDER; HUMAN; INFERTILITY THERAPY; MALE INFERTILITY; MENTAL STRESS; NUTRITION; PERSISTENT ORGANIC POLLUTANT; PRIORITY JOURNAL; REVIEW; SEMINAL TRACT INFECTION; SEMINAL VESICLE; SOCIAL STRESS; SPERM; SPERMATOGENESIS; ADULT; CHEMISTRY; GENETIC EPIGENESIS; GENETICS; MALE; PATHOLOGY; SPERMATOZOON;

ADULT; DNA METHYLATION; EPIGENESIS, GENETIC; GENOMIC IMPRINTING; HUMANS; INFERTILITY, MALE; MALE; SPERMATOZOA;

EID: 84937828677     PISSN: 09143505     EISSN: 17414520     Source Type: Journal    
DOI: 10.1111/cga.12113     Document Type: Review

References (131)

1. Allegrucci C, Thurston A, Lucas E, Young L. 2005. Epigenetics and the germline. Reproduction 129:137-149.
2. Andrews SC, Wood MD, Tunster SJ, Barton SC, Surani MA, John RM. 2007. Cdkn1c (p57Kip2) is the major regulator of embryonic growth within its imprinted domain on mouse distal chromosome 7. BMC Dev Biol 7:53.
3. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-1469.
4. Aoki VW, Liu L, Carrell DT. 2005. Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum Reprod 20:1298-1306.
5. Baarends WM, Hoogerbrugge JW, Roest HP etal. 1999. Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 207:322-333.
6. Bale TL. 2014. Lifetime stress experience: transgenerational epigenetics and germ cell programming. Dialogues Clin Neurosci 16:297-305.
7. Balhorn R, Reed S, Tanphaichitr N. 1988. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 44:52-55.
8. Barlow DP, Bartolomei MS. 2014. Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6:a018382.
9. Barton SC, Surani MA, Norris ML. 1984. Role of paternal and maternal genomes in mouse development. Nature 311:374-376.
10. Belokopytova IA, Kostyleva EI, Tomilin AN, Vorob'ev VI. 1993. Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin. Mol Reprod Dev 34:53-57.
11. Benchaib M, Ajina M, Lornage J, Niveleau A, Durand P, Guerin JF. 2003. Quantitation by image analysis of global DNA methylation in human spermatozoa and its prognostic value in in vitro fertilization: a preliminary study. Fertil Steril 80:947-953.
12. Bezold G, Politch JA, Kiviat NB, Kuypers JM, Wolff H, Anderson DJ. 2007. Prevalence of sexually transmissible pathogens in semen from asymptomatic male infertility patients with and without leukocytospermia. Fertil Steril 87:1087-1097.
13. Bliek J, Terhal P, van den Bogaard MJ etal. 2006. Hypomethylation of the H19 gene causes not only Silver-Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. Am J Hum Genet 78:604-614.
14. Boissonnas CC, Abdalaoui HE, Haelewyn V etal. 2010. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 18:73-80.
15. Boissonnas CC, Jouannet P, Jammes H. 2013. Epigenetic disorders and male subfertility. Fertil Steril 99:624-631.
16. Bonaldi A, Mazzeu JF, Costa SS etal. 2011. Microduplication of the ICR2 domain at chromosome 11p15 and familial Silver-Russell syndrome. Am J Med Genet A 155A:2479-2483.
17. Bonde JP, Toft G, Rylander L etal. 2008. Fertility and markers of male reproductive function in Inuit and European populations spanning large contrasts in blood levels of persistent organochlorines. Environ Health Perspect 116:269-277.
18. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536-2539.
19. Bowdin S, Allen C, Kirby G etal. 2007. A survey of assisted reproductive technology births and imprinting disorders. Hum Reprod 22:3237-3240.
20. Buiting K. 2010. Prader-Willi syndrome and Angelman syndrome. Am J Med Genet C Semin Med Genet 154C:365-376.
21. Carone BR, Fauquier L, Habib N etal. 2010. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084-1096.
22. Carrell DT, Emery BR, Hammoud S. 2007. Altered protamine expression and diminished spermatogenesis: what is the link? Hum Reprod Update 13:313-327.
23. Carrell DT, Emery BR, Liu L. 1999. Characterization of aneuploidy rates, protamine levels, ultrastructure, and functional ability of round-headed sperm from two siblings and implications for intracytoplasmic sperm injection. Fertil Steril 71:511-516.
24. Carrell DT, Liu L. 2001. 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 22:604-610.
25. Chang AS, Moley KH, Wangler M, Feinberg AP, Debaun MR. 2005. Association between Beckwith-Wiedemann syndrome and assisted reproductive technology: a case series of 19 patients. Fertil Steril 83:349-354.
26. Chevaillier P, Mauro N, Feneux D, Jouannet P, David G. 1987. Anomalous protein complement of sperm nuclei in some infertile men. Lancet 2:806-807.
27. Chiba H, Hiura H, Okae H etal. 2013. DNA methylation errors in imprinting disorders and assisted reproductive technology. Pediatr Int 55:542-549.
28. Cho C, Willis WD, Goulding EH etal. 2001. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 28:82-86.
29. Cleaton MA, Edwards CA, Ferguson-Smith AC. 2014. Phenotypic outcomes of imprinted gene models in mice: elucidation of pre- and postnatal functions of imprinted genes. Annu Rev Genomics Hum Genet 15:93-126.
30. Cox GF, Burger J, Lip V etal. 2002. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet 71:162-164.
31. Cumming JA, Carrell DT. 2009. Utility of reflexive semen cultures for detecting bacterial infections in patients with infertility and leukocytospermia. Fertil Steril 91:1486-1488.
32. Dada R, Kumar M, Jesudasan R, Fernandez JL, Gosalvez J, Agarwal A. 2012. Epigenetics and its role in male infertility. J Assist Reprod Genet 29:213-223.
33. Davis TL, Trasler JM, Moss SB, Yang GJ, Bartolomei MS. 1999. Acquisition of the H19 methylation imprint occurs differentially on the parental alleles during spermatogenesis. Genomics 58:18-28.
34. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. 2000. The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum Mol Genet 9:2885-2894.
35. DeBaun MR, Niemitz EL, Feinberg AP. 2003. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet 72:156-160.
36. DeChiara TM, Robertson EJ, Efstratiadis A. 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849-859.
37. Dohle GR, Halley DJ, Van Hemel JO etal. 2002. Genetic risk factors in infertile men with severe oligozoospermia and azoospermia. Hum Reprod 17:13-16.
38. Doornbos ME, Maas SM, McDonnell J, Vermeiden JP, Hennekam RC. 2007. Infertility, assisted reproduction technologies and imprinting disturbances: a Dutch study. Hum Reprod 22:2476-2480.
39. El Hajj N, Zechner U, Schneider E, Tresch A, Gromoll J, Hahn T, Schorsch M, Haaf T. 2011. Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev 5:60-69.
40. Emiliani S, Van den Bergh M, Vannin AS, Biramane J, Verdoodt M, Englert Y. 2000. Increased sperm motility after in-vitro culture of testicular biopsies from obstructive azoospermic patients results in better post-thaw recovery rate. Hum Reprod 15:2371-2374.
41. Fernandes S, Huellen K, Goncalves J etal. 2002. High frequency of DAZ1/DAZ2 gene deletions in patients with severe oligozoospermia. Mol Hum Reprod 8:286-298.
42. Gabory A, Ferry L, Fajardy I etal. 2012. Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS ONE 7:e47986.
43. Galli-Tsinopoulou A, Emmanouilidou E, Karagianni P, Grigoriadou M, Kirkos J, Varlamis GS. 2008. A female infant with Silver Russell Syndrome, mesocardia and enlargement of the clitoris. Hormones (Athens) 7:77-81.
44. Gianotten J, van der Veen F, Alders MP etal. 2003. Chromosomal region 11p15 is associated with male factor subfertility. Mol Hum Reprod 9:587-592.
45. Gicquel C, Gaston V, Mandelbaum J, Siffroi JP, Flahault A, Le Bouc Y. 2003. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am J Hum Genet 72:1338-1341.
46. Gold JA, Ruth C, Osann K etal. 2014. Frequency of Prader-Willi syndrome in births conceived via assisted reproductive technology. Genet Med 16:164-169.
47. Gosden R, Trasler J, Lucifero D, Faddy M. 2003. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 361:1975-1977.
48. Govarts E, Nieuwenhuijsen M, Schoeters G etal. 2012. Birth weight and prenatal exposure to polychlorinated biphenyls (PCBs) and dichlorodiphenyldichloroethylene (DDE): a meta-analysis within 12 European Birth Cohorts. Environ Health Perspect 120:162-170.
49. Guo YL, Hsu PC, Hsu CC, Lambert GH. 2000. Semen quality after prenatal exposure to polychlorinated biphenyls and dibenzofurans. Lancet 356:1240-1241.
50. Halliday J, Oke K, Breheny S, Algar E, Amor DJ. 2004. Beckwith-Wiedemann syndrome and IVF: a case-control study. Am J Hum Genet 75:526-528.
51. Hammoud SS, Purwar J, Pflueger C, Cairns BR, Carrell DT. 2010. Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 94:1728-1733.
52. Hartmann S, Bergmann M, Bohle RM, Weidner W, Steger K. 2006. Genetic imprinting during impaired spermatogenesis. Mol Hum Reprod 12:407-411.
53. Hata K, Okano M, Lei H, Li E. 2002. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129:1983-1993.
54. Haugen V, Pechacek J, Maher T, Wilde J, Kula L, Powell J. 2011. Decreasing pressure ulcer risk during hospital procedures: a rapid process improvement workshop. J Wound Ostomy Continence Nurs 38:155-159.
55. Hayashi K, Yoshida K, Matsui Y. 2005. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438:374-378.
56. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. 2006. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11:353-361.
57. Hiura H, Okae H, Chiba H etal. 2014. Imprinting methylation errors in ART. Reprod Med Biol 13:193-202.
58. Hiura H, Okae H, Miyauchi N, Sato F, Sato A, Van De Pette M, John RM, Kagami M, Nakai K, Soejima H, Ogata T, Arima T. 2012. Characterization of DNA methylation errors in patients with imprinting disorders conceived by assisted reproduction technologies. Hum Reprod 27:2541-2548.
59. Honda S, Weigel A, Hjelmeland LM, Handa JT. 2001. Induction of telomere shortening and replicative senescence by cryopreservation. Biochem Biophys Res Commun 282:493-498.
60. Horsthemke B, Buiting K. 2006. Imprinting defects on human chromosome 15. Cytogenet Genome Res 113:292-299.
61. Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, Sokol RZ. 2007. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS ONE 2:e1289.
62. Jacob KJ, Robinson WP, Lefebvre L. 2013. Beckwith-Wiedemann and Silver-Russell syndromes: opposite developmental imbalances in imprinted regulators of placental function and embryonic growth. Clin Genet 84:326-334.
63. John RM, Lefebvre L. 2011. Developmental regulation of somatic imprints. Differentiation 81:270-280.
64. Kagami M, Nagai T, Fukami M, Yamazawa K, Ogata T. 2007. Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet 24:131-136.
65. Kallen B, Finnstrom O, Lindam A, Nilsson E, Nygren KG, Otterblad PO. 2010. Congenital malformations in infants born after in vitro fertilization in Sweden. Birth Defects Res A Clin Mol Teratol 88:137-143.
66. Kaneda A, Wakazono K, Tsukamoto T etal. 2004. Lysyl oxidase is a tumor suppressor gene inactivated by methylation and loss of heterozygosity in human gastric cancers. Cancer Res 64:6410-6415.
67. Keck C, Gerber-Schafer C, Clad A, Wilhelm C, Breckwoldt M. 1998. Seminal tract infections: impact on male fertility and treatment options. Hum Reprod Update 4:891-903.
68. Kerjean A, Dupont JM, Vasseur C, Le Tessier D, Cuisset L, Paldi A, Jouannet P, Jeanpierre M. 2000. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet 9:2183-2187.
69. Kobayashi H, Hiura H, John RM etal. 2009. DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. Eur J Hum Genet 17:1582-1591.
70. Kobayashi H, Sato A, Otsu E etal. 2007. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 16:2542-2551.
71. Kondrashov A. 2012. Genetics: the rate of human mutation. Nature 488:467-468.
72. Korrovits P, Ausmees K, Mandar R, Punab M. 2008. Prevalence of asymptomatic inflammatory (National Institutes of Health Category IV) prostatitis in young men according to semen analysis. Urology 71:1010-1015.
73. Lee J, Inoue K, Ono R etal. 2002. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129:1807-1817.
74. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. 1995. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature 375:34-39.
75. Li JY, Lees-Murdock DJ, Xu GL, Walsh CP. 2004. Timing of establishment of paternal methylation imprints in the mouse. Genomics 84:952-960.
76. Ligon BL. 2005. Albert Ludwig Sigesmund Neisser: discoverer of the cause of gonorrhea. Semin Pediatr Infect Dis 16:336-341.
77. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. 2005. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382-1386.
78. Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC. 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.
79. Lim D, Bowdin SC, Tee L, Kirby GA, Blair E, Fryer A, Lam W, Oley C, Cole T, Brueton LA, Reik W, Macdonald F, Maher ER. 2009. Clinical and molecular genetic features of Beckwith-Wiedemann syndrome associated with assisted reproductive technologies. Hum Reprod 24:741-747.
80. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. 2004. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 13:839-849.
81. Ludwig M, Katalinic A, Gross S, Sutcliffe A, Varon R, Horsthemke B. 2005. Increased prevalence of imprinting defects in patients with Angelman syndrome born to subfertile couples. J Med Genet 42:289-291.
82. MacLennan NK, James SJ, Melnyk S etal. 2004. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol Genomics 18:43-50.
83. Maher ER. 2005. Imprinting and assisted reproductive technology. Hum Mol Genet 14:Spec No 1: R133-R138.
84. Maher ER, Brueton LA, Bowdin SC etal. 2003. Beckwith-Wiedemann syndrome and assisted reproduction technology (ART). J Med Genet 40:62-64.
85. Manning M, Lissens W, Liebaers I, Van Steirteghem A, Weidner W. 2001. Imprinting analysis in spermatozoa prepared for intracytoplasmic sperm injection (ICSI). Int J Androl 24:87-94.
86. Marques CJ, Carvalho F, Sousa M, Barros A. 2004. Genomic imprinting in disruptive spermatogenesis. Lancet 363:1700-1702.
87. Marques CJ, Costa P, Vaz B etal. 2008. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 14:67-74.
88. Marques CJ, Francisco T, Sousa S, Carvalho F, Barros A, Sousa M. 2010. Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril 94:585-594.
89. McAuliffe ME, Williams PL, Korrick SA, Dadd R, Perry MJ. 2012. The association between sperm sex chromosome disomy and semen concentration, motility and morphology. Hum Reprod 27:2918-2926.
90. McGrath J, Solter D. 1984. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179-183.
91. Meaney MJ, Szyf M, Seckl JR. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol Med 13:269-277.
92. Meeker JD, Ehrlich S, Toth TL etal. 2010. Semen quality and sperm DNA damage in relation to urinary bisphenol A among men from an infertility clinic. Reprod Toxicol 30:532-539.
93. Milagro FI, Campion J, Garcia-Diaz DF, Goyenechea E, Paternain L, Martinez JA. 2009. High fat diet-induced obesity modifies the methylation pattern of leptin promoter in rats. J Physiol Biochem 65:1-9.
94. Miura K, Niikawa N. 2005. Do monochorionic dizygotic twins increase after pregnancy by assisted reproductive technology? J Hum Genet 50:1-6.
95. Moll AC, Imhof SM, Cruysberg JR, Schouten-van Meeteren AY, Boers M, van Leeuwen FE. 2003. Incidence of retinoblastoma in children born after in-vitro fertilisation. Lancet 361:309-310.
96. Morgan HD, Santos F, Green K, Dean W, Reik W. 2005. Epigenetic reprogramming in mammals. Hum Mol Genet 14:Spec No 1: R47-R58.
97. Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, Goncalves J, Plancha CE. 2010. Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 25:2647-2654.
98. Niemitz EL, Feinberg AP. 2004. Epigenetics and assisted reproductive technology: a call for investigation. Am J Hum Genet 74:599-609.
99. Obata Y, Kono T. 2002. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J Biol Chem 277:5285-5289.
100. Orstavik KH, Eiklid K, van der Hagen CB etal. 2003. Another case of imprinting defect in a girl with Angelman syndrome who was conceived by intracytoplasmic semen injection. Am J Hum Genet 72:218-219.
101. Poplinski A, Tuttelmann F, Kanber D, Horsthemke B, Gromoll J. 2010. Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int J Androl 33:642-649.
102. Rakyan VK, Chong S, Champ ME etal. 2003. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci U S A 100:2538-2543.
103. Razavi S, Nasr-Esfahani MH, Mardani M, Mafi A, Moghdam A. 2003. Effect of human sperm chromatin anomalies on fertilization outcome post-ICSI. Andrologia 35:238-243.
104. Richthoff J, Rylander L, Jonsson BA etal. 2003. Serum levels of 2, 2′, 4, 4′, 5, 5′-hexachlorobiphenyl (CB-153) in relation to markers of reproductive function in young males from the general Swedish population. Environ Health Perspect 111:409-413.
105. Rossignol S, Steunou V, Chalas C etal. 2006. The epigenetic imprinting defect of patients with Beckwith-Wiedemann syndrome born after assisted reproductive technology is not restricted to the 11p15 region. J Med Genet 43:902-907.
106. Roth TL, Zoladz PR, Sweatt JD, Diamond DM. 2011. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. J Psychiatr Res 45:919-926.
107. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. 2005. Establishment of male-specific epigenetic information. Gene 345:139-153.
108. Sato A, Hiura H, Okae H etal. 2011. Assessing loss of imprint methylation in sperm from subfertile men using novel methylation polymerase chain reaction Luminex analysis. Fertil Steril 95:129-134, 134 e1-4.
109. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. 2007. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 22:26-35.
110. Shimizu Y, Fukuda J, Sato W, Kumagai J, Hirano H, Tanaka T. 2004. First-trimester diagnosis of conjoined twins after in-vitro fertilization-embryo transfer (IVF-ET) at blastocyst stage. Ultrasound Obstet Gynecol 24:208-209.
111. Sun JX, Helgason A, Masson G etal. 2012. A direct characterization of human mutation based on microsatellites. Nat Genet 44:1161-1165.
112. Surani MA. 1998. Imprinting and the initiation of gene silencing in the germ line. Cell 93:309-312.
113. Surani MA, Barton SC, Norris ML. 1984. Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548-550.
114. Sutcliffe AG, Peters CJ, Bowdin S, Temple K, Reardon W, Wilson L, Clayton-Smith J, Brueton LA, Bannister W, Maher ER. 2006. Assisted reproductive therapies and imprinting disorders - a preliminary British survey. Hum Reprod 21:1009-1011.
115. Svensson J, Bjornstahl A, Ivarsson SA. 2005. Increased risk of Silver-Russell syndrome after in vitro fertilization? Acta Paediatr 94:1163-1165.
116. Thompson JR, Williams CJ. 2005. Genomic imprinting and assisted reproductive technology: connections and potential risks. Semin Reprod Med 23:285-295.
117. Tilghman SM. 1999. The sins of the fathers and mothers: genomic imprinting in mammalian development. Cell 96:185-193.
118. Toft G, Guillette LJ, Jr. 2005. Decreased sperm count and sexual behavior in mosquitofish exposed to water from a pesticide-contaminated lake. Ecotoxicol Environ Saf 60:15-20.
119. Toft G, Rignell-Hydbom A, Tyrkiel E etal. 2006. Semen quality and exposure to persistent organochlorine pollutants. Epidemiology 17:450-458.
120. Tunster SJ, Van de Pette M, John RM. 2011. Fetal overgrowth in the Cdkn1c mouse model of Beckwith-Wiedemann syndrome. Dis Model Mech 4:814-821.
121. Ueda T, Abe K, Miura A etal. 2000. The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 5:649-659.
122. Ushijima T, Nakajima T, Maekita T. 2006. DNA methylation as a marker for the past and future. J Gastroenterol 41:401-407.
123. van Montfoort AP, Hanssen LL, de Sutter P, Viville S, Geraedts JP, de Boer P. 2012. Assisted reproduction treatment and epigenetic inheritance. Hum Reprod Update 18:171-197.
124. Vucetic Z, Kimmel J, Reyes TM. 2011. Chronic high-fat diet drives postnatal epigenetic regulation of mu-opioid receptor in the brain. Neuropsychopharmacology 36:1199-1206.
125. Waterland RA, Jirtle RL. 2003. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23:5293-5300.
126. Waterland RA, Jirtle RL. 2004. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition 20:63-68.
127. Waterland RA, Lin JR, Smith CA, Jirtle RL. 2006. Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet 15:705-716.
128. Weaver IC, Cervoni N, Champagne FA etal. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
129. Weber M, Hellmann I, Stadler MB etal. 2007. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466.
130. Wolff GL, Roberts DW, Mountjoy KG. 1999. Physiological consequences of ectopic agouti gene expression: the yellow obese mouse syndrome. Physiol Genomics 1:151-163.
131. Wolff H. 1995. The biologic significance of white blood cells in semen. Fertil Steril 63:1143-1157.