Indices of methylation in sperm DNA from fertile men differ between distinct geographical regions

Human Reproduction

Volumn 29, Issue 9, 2014, Pages 2065-2072

  Consales, C ^a   Leter, G ^a   Bonde, J P E ^b   Toft, G ^c   Eleuteri, P ^a   Moccia, T ^d   Budillon, A ^d   Jonsson B A G ^e   Giwercman, A ^f   Pedersen, H S ^g   Ludwicki, J K ^h   Zviezdai, V ⁱ   Heederik, D ^j   Spano M ^a  

^a ENEA C R CASACCIA   (Italy)

^b BISPEBJERG HOSPITAL   (Denmark)

^c AARHUS UNIVERSITY HOSPITAL   (Denmark)

^d NATIONAL CANCER INSTITUTE   (Italy)

^e LUND UNIVERSITY   (Sweden)

^f LUND UNIVERSITY HOSPITAL   (Sweden)

^g GREENLAND INSTITUTE OF NATURAL RESOURCES   (Greenland)

^h NATIONAL INSTITUTE OF HYGIENE   (Poland)

ⁱ KHARKIV NATIONAL MEDICAL UNIVERSITY   (Ukraine)

^j UTRECHT UNIVERSITY   (Netherlands)

more..

Author keywords

epidemiology; flow cytometry; human spermatozoa; pyrosequencing; sperm DNA methylation

Indexed keywords

5 METHYLCYTOSINE; DNA; MONOCLONAL ANTIBODY; REPETITIVE DNA; SEX HORMONE;

ALCOHOL CONSUMPTION; ARTICLE; BODY MASS; CHROMATIN; CROSS-SECTIONAL STUDY; DNA METHYLATION; DNA SEQUENCE; FLOW CYTOMETRY; GREENLAND; HORMONE BLOOD LEVEL; HUMAN; LEUKOCYTE COUNT; MALE; MALE FERTILITY; MALE GENITAL TRACT PARAMETERS; NORMAL HUMAN; PERIPHERAL LYMPHOCYTE; POLAND; SEQUENCE ANALYSIS; SPERM; UKRAINE; COMPARATIVE STUDY; FERTILITY; GENETICS; GEOGRAPHY; HUMAN GENOME; METABOLISM; NUCLEOTIDE REPEAT; SEMEN ANALYSIS; SPERMATOZOON;

CROSS-SECTIONAL STUDIES; DNA; DNA METHYLATION; FERTILITY; GENOME, HUMAN; GEOGRAPHY; GREENLAND; HUMANS; MALE; POLAND; REPETITIVE SEQUENCES, NUCLEIC ACID; SEMEN ANALYSIS; SPERMATOZOA; UKRAINE;

EID: 84906093926     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deu176     Document Type: Article

References (52)

1. Alegría-Torres JA, Baccarelli A, Bollati V. Epigenetics and lifestyle. Epigenomics 2011;3:267-277.
2. Ankolkar M, Salvi V, Warke H, Vundinti BR, Balasinor NH. Methylation status of imprinted genes DLK1-GTL2, MEST (PEG1), ZAC (PLAGL1), and LINE-1 elements in spermatozoa of normozoospermic men, unlike H19 imprinting control regions, is not associated with idiopathic recurrent spontaneous miscarriages. Fertil Steril 2013;99:1668-1673.
3. Aoki VW, Emery BR, Carrell DT. Global sperm deoxyribonucleic acid methylation is unaffected in protamine-deficient infertile males. Fertil Steril 2006;86:1541-1543. (Pubitemid 44602048)
4. Barzideh J, Scott RJ, Aitken RJ. Analysis of the global methylation status of human spermatozoa and its association with the tendency of these cells to enter apoptosis. Andrologia 2013;45:424-429.
5. Benchaib M, Ajina M, Lornage J, Niveleau A, Durand P, Guérin 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;80:947-953. (Pubitemid 37230032)
6. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A, Guérin JF. Influence of global sperm DNA methylation on IVF results. Hum Reprod 2005;20:768-773. (Pubitemid 40425507)
7. Boissonnas CC, Abdalaoui HE, Haelewyn V, Fauque P, Dupont JM, Gut I, Vaiman D, Jouannet P, Tost J, Jammes H. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 2010;18:73-80.
8. Boissonnas CC, Jouannet P, Jammes H. Epigenetic disorders and male subfertility. Fertil Steril 2013;99:624-631.
9. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 2007; 67:876-880.
10. Bollati V, Fabris S, Pegoraro V, Ronchetti D, Mosca L, Deliliers GL, Motta V, Bertazzi PA, Baccarelli A, Neri A. Differential repetitive DNA methylation in multiple myeloma molecular subgroups. Carcinogenesis 2009; 30:1330-1335.
11. BollatiV, Galimberti D, Pergoli L, Dalla Valle E, Barretta F, Cortini F, Scarpini E, Bertazzi PA, Baccarelli A. DNA methylation in repetitive elements and Alzheimer disease. Brain Behav Immun 2011;25:1078-1083.
12. Bonde JP, Toft G, Rylander L, Rignell-Hydbom A, Giwercman A, Spanò M, Manicardi GC, Bizzaro D, Ludwicki JK, Zvyezday V et al. Fertility and markers of male reproductive function in Inuit and European populations spanning large contrasts in blood levels of persistent organochlorines. Environ Health Perspect 2008;116:269-277. (Pubitemid 351395591)
13. Carrell DT. Epigenetics of the male gamete. Fertil Steril 2012;97:267-274.
14. Casa V, Gabellini D. A repetitive elements perspective in Polycomb epigenetics. Front Genet 2012;3:199.
15. Cortessis VK, Siegmund K, Houshdaran S, Laird PW, Sokol RZ. Repeated assessment by high-throughput assay demonstrates that sperm DNA methylation levels are highly reproducible. Fertil Steril 2011; 96:1325-1330.
16. Daxinger L, Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet 2012;13:153-162.
17. Denis H, Ndlovu MN, Fuks F. Regulation of mammalian DNA methyltransferases: a route to new mechanisms. EMBO Rep 2011; 12:647-656.
18. Di Giacomo M, Comazzetto S, Saini H, De Fazio S, Carrieri C, Morgan M, Vasiliauskaite L, Benes V, Enright AJ, O'Carroll D. Multiple epigenetic mechanisms and the piRNA pathway enforce LINE1 silencing during adult spermatogenesis. Mol Cell 2013;50:601-608.
19. El Hajj N, Zechner U, Schneider E, Tresch A, Gromoll J, Hahn T, Schorsch M, Haaf T. Methylation status of imprinted genes and repetitive elements in sperm DNA from infertile males. Sex Dev 2011;5:60-69.
20. EvensonDP, Larson KL, Jost LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 2002;23:25-43. (Pubitemid 34001126)
21. Fabris S, Bollati V, Agnelli L, Morabito F, Motta V, Cutrona G, Matis S, Grazia Recchia A, Gigliotti V, Gentile M et al. Biological and clinical relevance of quantitative global methylation of repetitive DNA sequences in chronic lymphocytic leukemia. Epigenetics 2011;6:188-194.
22. Faulk C, Dolinoy DC. Timing is everything: the when and how of environmentally induced changes in the epigenome of animals. Epigenetics 2011;6:791-797.
23. Feil R, Fraga MF. Epigenetics and the environment: emerging patterns and implications. Nat Rev Genet 2012;13:97-109.
24. Furrow RE, Christiansen FB, Feldman MW. Environment-sensitive epigenetics and the heritability of complex diseases. Genetics 2011; 189:1377-1187.
25. Giwercman A, Rylander L, Rignell-Hydbom A, Jönsson BA, Pedersen HS, Ludwicki JK, Lesovoy V, Zvyezday V, Spano M, Manicardi GC et al. Androgen receptor gene CAG repeat length as amodifier of the association between persistent organohalogen pollutant exposure markers and semen characteristics. Pharmacogenet Genomics 2007;17:391-401. (Pubitemid 46763384)
26. Giwercman C, Giwercman A, Pedersen HS, Toft G, Lundin K, Bonde JP, Lundberg Giwercman Y. Polymorphisms in genes regulating androgen activity among prostate cancer low-risk Inuit men and high-risk Scandinavians. Int J Androl 2008;31:25-30.
27. Guerrero-Bosagna C, Skinner MK. Environmentally induced epigenetic transgenerational inheritance of phenotype and disease. Mol Cell Endocrinol 2012;354:3-8.
28. Hou L, Zhang X, Wang D, Baccarelli A. Environmental chemical exposures and human epigenetics. Int J Epidemiol 2012;41:79-105.
29. Kläver R, Bleiziffer A, Redmann K, Mallidis C, Kliesch S, Gromoll J. Routine cryopreservation of spermatozoa is safe - evidence from the DNA methylation pattern of nine spermatozoa genes. J Assist Reprod Genet 2012;29:943-950.
30. Kläver R, Tüttelmann F, Bleiziffer A, Haaf T, Kliesch S, Gromoll J. DNA methylation in spermatozoa as a prospective marker in andrology. Andrology 2013;1:731-740.
31. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, Sasaki H, Yaegashi N, Arima T. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 2007;16:2542-2551. (Pubitemid 47617721)
32. Krausz C, Sandoval J, Sayols S, Chianese C, Giachini C, Heyn H, Esteller M. Novel insights into DNA methylation features in spermatozoa: stability and peculiarities. PLoS One 2012;7:e44479.
33. Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, Suderman M, Hallett M, Kimmins S. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun 2013;4:2889.
34. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A, Sousa M. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 2008;14:67-73. (Pubitemid 351321167)
35. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 2011;146:1029-1041.
36. Peluso M, Bollati V, Munnia A, Srivatanakul P, Jedpiyawongse A, Sangrajrang S, Piro S, Ceppi M, Bertazzi PA, Boffetta P et al. DNA methylation differences in exposed workers and nearby residents of the Ma Ta Phut industrial estate, Rayong, Thailand. Int J Epidemiol 2012; 41:1753-1760.
37. Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 2008;9:129-140.
38. Seisenberger S, Popp C, Reik W. Retrotransposons and germ cells: reproduction, death, and diversity. F1000 Biol Rep 2010;2:44.
39. Seisenberger S, Peat JR, Hore TA, Santos F, Dean W, Reik W. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos Trans R Soc Lond B Biol Sci 2013; 368:20110330.
40. Sharpe RM. Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010;365:1697-1712.
41. Spanò M, Toft G, Hagmar L, Eleuteri P, Rescia M, Rignell-Hydbom A, Tyrkiel E, Zvyezday V, Bonde JP; INUENDO. Exposure to PCB and p, p'-DDE in European and Inuit populations: impact on human sperm chromatin integrity. Hum Reprod 2005;20:3488-3499. (Pubitemid 41742532)
42. StronatiA, ManicardiGC, CecatiM, BordicchiaM, Ferrante L, Spanò M, ToftG, Bonde JP, Jönsson BA, Rignell-Hydbom A et al. Relationships between sperm DNA fragmentation, sperm apoptotic markers and serum levels of CB-153 and p, p'-DDE in European and Inuit populations. Reproduction 2006;132:949-958. (Pubitemid 46040665)
43. Tavalaee M, Razavi S, Nasr-Esfahani MH. Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril 2009;91:1119-1126.
44. Toft G, Rignell-Hydbom A, Tyrkiel E, Shvets M, Giwercman A, Lindh CH, Pedersen HS, Ludwicki JK, Lesovoy V, Hagmar L et al. Semen quality and exposure to persistent organochlorine pollutants. Epidemiology 2006; 17:450-458. (Pubitemid 44305519)
45. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nat Protoc 2007;2:2265-2275. (Pubitemid 351575045)
46. Trasler JM. Epigenetics in spermatogenesis. Mol Cell Endocrinol 2009; 306:33-36.
47. Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009;26:537-544.
48. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, LairdPW. Analysis of repetitive elementDNAmethylation by MethyLight. Nucleic Acids Res 2005;33:6823-6836. (Pubitemid 41830488)
49. WHO, World Health Organization. WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction, 4th edn. Cambridge, UK: Cambridge University Press, 1999.
50. Yamagata K, Yamazaki T, Miki H, Ogonuki N, Inoue K, Ogura A, Baba T. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev Biol 2007; 312:419-426. (Pubitemid 350180767)
51. Yang AS, Estécio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 2004;32:e38.
52. Zhu ZZ, Hou L, Bollati V, Tarantini L, Marinelli B, Cantone L, Yang AS, Vokonas P, Lissowska J, Fustinoni S et al. Predictors of global methylation levels in blood DNA of healthy subjects: a combined analysis. Int J Epidemiol 2012;41:126-139.