Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm

PLoS ONE

Volumn 2, Issue 12, 2007, Pages

  Houshdaran, Sahar ^a   Cortessis, Victoria K ^a   Siegmund, Kimberly ^a   Yang, Allen ^a   Laird, Peter W ^a   Sokol, Rebecca Z ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CELL ASSAY; CELL STRUCTURE; CONTROLLED STUDY; DNA DETERMINATION; DNA ISOLATION; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENETIC DISORDER; GERM LINE; HUMAN; HUMAN CELL; ILLUMINATION; MAJOR CLINICAL STUDY; MALE; PATHOPHYSIOLOGY; PURIFICATION; SPERMATOZOON ABNORMALITY; SPERMATOZOON COUNT; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; GENETIC EPIGENESIS; GERM CELL; METABOLISM; MIDDLE AGED; SPERMATOZOON;

ADULT; DNA METHYLATION; EPIGENESIS, GENETIC; GERM CELLS; HUMANS; MALE; MIDDLE AGED; SPERMATOZOA;

EID: 44949259146     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001289     Document Type: Article

References (81)

1. Abma JC, Chandra A, Mosher WD, Peterson LS, Piccinino LJ (1997) Fertility, family planning, and women's health: new data from the 1995 National Survey of Family Growth. Vital Health Stat 23(19): 1-114.
2. Chandra A, Stephen EH (1998) Impaired fecundity in the United States: 1982-1995. Fam Plann Perspect 30(1): 34-42.
3. Ventura SJ, Mosher WD, Curtin SC, Abma JC, Henshaw S (1999) Highlights of trends in pregnancies and pregnancy rates by outcome: estimates for the United States, 1976-96. Natl Vital Stat Rep 47(29): 1-9.
4. http://www.cdc.gov/ART/ART2004/faq.htm#1.
5. http://www.cdc.gov/nchs/.
6. http://www.cdc.gov/nchs/products/pubs/pubd/series/sr23/pre-1/sr23_25.htm.
7. Thonneau P, Marchand S, Tallec A, Ferial ML, Ducot B, et al. (1991) Incidence and main causes of infertility in a resident population (1,850,000) of three French regions (1988-1989). Hum Reprod 6(6): 811-816.
8. Maduro MR, Lo KC, Chuang WW, Lamb DJ (2003) Genes and male infertility: what can go wrong? J Androl 24(4): 485-493.
9. McElreavey K, Krausz C, Bishop CE (2000) The human Y chromosome and male infertility. Results Probl Cell Differ 28: 211-232.
10. Sharlip ID, Jarow JP, Belker AM, Lipshultz LI, Sigman M, et al. (2002) Best practice policies for male infertility. Fertil Steril 77(5): 873-882.
11. Sokol RZ (1997) male factor in male infertility. In: Lobo R. MD, Paulson R, eds. Infertility, Contraception, and Reproductive Endocrinology. Madden, MA: Blackwell Sciene, Inc. pp 547-566.
12. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, et al. (2005) Establishment of male-specific epigenetic information. Gene 345(2): 139-153.
13. Emery BR, Carrell DT (2006) The effect of epigenetic sperm abnormalities on early embryogenesis. Asian J Androl 8(2): 131-142.
14. Li E (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3(9): 662-673.
15. Saitou M, Barton SC, Surani MA (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418(6895): 293-300.
16. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127(6): 643-651.
17. Biermann K, Steger K (2007) Eipgenetics in Male Germ Cells. J Androl.
18. Ariel M, Cedar H, McCarrey J (1994) Developmental changes in methylation of spermatogenesis-specific genes include reprogramming in the epididymis. Nat Genet 7(1): 59-63.
19. Trasler JM (1998) Origin and roles of genomic methylation patterns in male germ cells. Semin Cell Dev Biol 9(4): 467-474.
20. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM (2007) A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A 104(1): 228-233.
21. Bestor TH, Bourc'his D (2004) Transposon silencing and imprint establishment in mammalian germ cells. Cold Spring Harb Symp Quant Biol 69: 381-387.
22. Schaefer CB, Ooi SK, Bestor TH, Bourc'his D (2007) Epigenetic decisions in mammalian germ cells. Science 316(5823): 398-399.
23. Flanagan JM, Popendikyte V, Pozdniakovaite N, Sobolev M, Assadzadeh A, et al. (2006) Intra- and interindividual epigenetic variation in human germ cells. Am J Hum Genet 79(1): 67-84.
24. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, et al. (2005) Influence of global sperm DNA methylation on IVF results. Hum Reprod 20(3): 768-773.
25. Hartmann S, Bergmann M, Bohle RM, Weidner W, Steger K (2006) Genetic imprinting during impaired spermatogenesis. Mol Hum Reprod 12(6): 407-411.
26. Marques CJ, Carvalho F, Sousa M, Barros A (2004) Genomic imprinting in disruptive spermatogenesis. Lancet 363(9422): 1700-1702.
27. 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(2): 87-94.
28. Varrault A, Bilanges B, Mackay DJ, Basyuk E, Ahr B, et al. (2001) Characterization of the methylation-sensitive promoter of the imprinted ZAC gene supports its role in transient neonatal diabetes mellitus. J Biol Chem. pp 18653-18656.
29. Weisenberger DJ, Siegmund KD, Campan M, Young J, Long TI, et al. (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38(7): 787-793.
30. Dale B, Elder K (1997) In vitro fertilization. New York: Cambridge University Press. 187 p.
31. Hayashi K, de Sousa Lopes SM, Surani MA (2007) Germ cell specification in mice. Science 316(5823): 394-396.
32. Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, Saitou M (2006) Gene expression dynamics during germline specification in mice identified by quantitative single-cell gene expression profiling. Biol Reprod 75(5): 705-716.
33. Surani MA, Hayashi K, Hajkova P (2007) Genetic and epigenetic regulators of pluripotency. Cell 128(4): 747-762.
34. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, et al. (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117(1-2): 15-23.
35. Li JY, Lees-Murdock DJ, Xu GL, Walsh CP (2004) Timing of establishment of paternal methylation imprints in the mouse. Genomics 84(6): 952-960.
36. Szabo PE, Hubner K, Scholer H, Mann JR (2002) Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech Dev 115(1-2): 157-160.
37. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, et al. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35(2): 88-93.
38. Lees-Murdock DJ, De Felici M, Walsh CP (2003) Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82(2): 230-237.
39. Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, et al. (2002) Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129(8): 1807-1817.
40. Yamazaki Y, Mann MR, Lee SS, Marh J, McCarrey JR, et al. (2003) Reprogramming of primordial germ cells begins before migration into the genital ridge, making these cells inadequate donors for reproductive cloning. Proc Natl Acad Sci U S A 100(21): 12207-12212.
41. Trasler JM (2006) Gamete imprinting: setting epigenetic patterns for the next generation. Reprod Fertil Dev 18(1-2): 63-69.
42. Morgan HD, Sutherland HG, Martin DI, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23(3): 314-318.
43. Kearns M, Preis J, McDonald M, Morris C, Whitelaw E (2000) Complex patterns of inheritance of an imprinted murine transgene suggest incomplete germline erasure. Nucleic Acids Res 28(17): 3301-3309.
44. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, et al. (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(5): 2538-2543.
45. Kerjean A, Dupont JM, Vasseur C, Le Tessier D, Cuisset L, et al. (2000) Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum Mol Genet 9(14): 2183-2187.
46. Cupp AS, Uzumcu M, Suzuki H, Dirks K, Phillips B, et al. (2003) Effect of transient embryonic in vivo exposure to the endocrine disruptor methoxychlor on embryonic and postnatal testis development. J Androl 24(5): 736-745.
47. Chang HS, Anway MD, Rekow SS, Skinner MK (2006) Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 147(12): 5524-5541.
48. Acacio BD, Gottfried T, Israel R, Sokol RZ (2000) Evaluation of a large cohort of men presenting for a screening semen analysis. Fertil Steril 73(3): 595-597.
49. (1999) World Health Organization Laboratory Manual for Human Semen and Sperm Cervical Mucus Interaction.
50. Guzick DS, Overstreet JW, Factor-Litvak P, Brazil CK, Nakajima ST, et al. (2001) Sperm morphology, motility, and concentration in fertile and infertile men. N Engl J Med 345(19): 1388-1393.
51. www.irvinesci.com (2006).
52. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, et al. (1991) Simplified mammalian DNA isolation procedure. Nucleic Acids Res 19(15): 4293.
53. Bibikova M, Lin Z, Zhou L, Chudin E, Garcia EW, et al. (2006) High-throughput DNA methylation profiling using universal bead arrays. Genome Res 16(3): 383-393.
54. www.illumina.com/pages.ilmn?ID =193 (2007).
55. http://www.illumina.com (2007).
56. Benjamini y, Hochberg y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. R Statist Soc B 57(1): 289-300.
57. Kaufman L, Rousseeuw PJ (1990) Finding Groups in Data: An introduction to cluster analysis. Wiley Series in Probability and Mathematical Statistics. New York: John Wiley & Sons, Inc.
58. www.geneimprint.com (2006).
59. Astuti D, Latif F, Wagner K, Gentle D, Cooper WN, et al. (2005) Epigenetic alteration at the DLK1-GTL2 imprinted domain in human neoplasia: analysis of neuroblastoma, phaeochromocytoma and Wilms' tumour. Br J Cancer 92(8): 1574-1580.
60. Bastepe M, Frohlich LF, Hendy GN, Indridason OS, Josse RG, et al. (2003) Autosomal dominant pseudohypoparathyroidism type Ib is associated with a heterozygous microdeletion that likely disrupts a putative imprinting control element of GNAS. J Clin Invest 112(8): 1255-1263.
61. Bastepe M, Frohlich LF, Linglart A, Abu-Zahra HS, Tojo K, et al. (2005) Deletion of the NESP55 differentially methylated region causes loss of maternal GNAS imprints and pseudohypoparathyroidism type Ib. Nat Genet 37(1): 25-27.
62. Bell AC, Felsenfeld G (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405(6785): 482-485.
63. de la Puente A, Hall J, Wu YZ, Leone G, Peters J, et al. (2002) Structural characterization of Rasgrf1 and a novel linked imprinted locus. Gene 291(1-2): 287-297.
64. Gaston V, Le Bouc Y, Soupre V, Burglen L, Donadieu J, et al. (2001) Analysis of the methylation status of the KCNQ1OT and H19 genes in leukocyte DNA for the diagnosis and prognosis of Beckwith-Wiedemann syndrome. Eur J Hum Genet 9(6): 409-418.
65. Higashimoto K, Soejima H, Saito T, Okumura K, Mukai T (2006) Imprinting disruption of the CDKN1C/KCNQ1OT1 domain: the molecular mechanisms causing Beckwith-Wiedemann syndrome and cancer. Cytogenet Genome Res 113(1-4): 306-312.
66. Jie X, Lang C, Jian Q, Chaoqun L, Dehua Y, et al. (2007) Androgen activates PEG10 to promote carcinogenesis in hepatic cancer cells. Oncogene.
67. Liu J, Nealon JG, Weinstein LS (2005) Distinct patterns of abnormal GNAS imprinting in familial and sporadic pseudohypoparathyroidism type IB. Hum Mol Genet 14(1): 95-102.
68. Murphy SK, Wylie AA, Jirtle RL (2001) Imprinting of PEG3, the human homologue of a mouse gene involved in nurturing behavior. Genomics 71(1): 110-117.
69. Runte M, Huttenhofer A, Gross S, Kiefmann M, Horsthemke B, et al. (2001) The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolar RNA species and as an antisense RNA for UBE3A. Hum Mol Genet 10(23): 2687-2700.
70. Runte M, Kroisel PM, Gillessen-Kaesbach G, Varon R, Horn D, et al. (2004) SNURF-SNRPN and UBE3A transcript levels in patients with Angelman syndrome. Hum Genet 114(6): 553-561.
71. Sutcliffe JS, Nakao M, Christian S, Orstavik KH, Tommerup N, et al. (1994) Deletions of a differentially methylated CpG island at the SNRPN gene define a putative imprinting control region. Nat Genet 8(1): 52-58.
72. Suzuki S, Ono R, Narita T, Pask AJ, Shaw G, et al. (2007) Retrotransposon silencing by DNA methylation can drive mammalian genomic imprinting. PLoS Genet 3(4): e55.
73. Vu TH, Li T, Nguyen D, Nguyen BT, Yao XM, et al. (2000) Symmetric and asymmetric DNA methylation in the human IGF2-H19 imprinted region. Genomics 64(2): 132-143.
74. Cui H, Onyango P, Brandenburg S, Wu Y, Hsieh CL, et al. (2002) Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res 62(22): 6442-6446.
75. Hancock AL, Brown KW, Moorwood K, Moon H, Holmgren C, et al. (2007) A CTCF-binding silencer regulates the imprinted genes AWT1 and WT1-AS and exhibits sequential epigenetic defects during Wilms' tumourigenesis. Hum Mol Genet 16(3): 343-354.
76. Kim JD, Hinz AK, Choo JH, Stubbs L, Kim J (2007) YY1 as a controlling factor for the Peg3 and Gnas imprinted domains. Genomics 89(2): 262-269.
77. Lin SP, Youngson N, Takada S, Seitz H, Reik W, et al. (2003) Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat Genet 35(1): 97-102.
78. Murrell A, Heeson S, Reik W (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36(8): 889-893.
79. Ono R, Kobayashi S, Wagatsuma H, Aisaka K, Kohda T, et al. (2001) A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73(2): 232-237.
80. Sullivan MJ, Taniguchi T, Jhee A, Kerr N, Reeve AE (1999) Relaxation of IGF2 imprinting in Wilms tumours associated with specific changes in IGF2 methylation. Oncogene 18(52): 7527-7534.
81. Yun J, Park CW, Lee YJ, Chung JH (2003) Allele-specific methylation at the promoter-associated CpG island of mouse Copg2. Mamm Genome 14(6): 376-382.