Promoter targeted bisulfite sequencing reveals DNA methylation profiles associated with low sperm motility in asthenozoospermia

Human Reproduction

Volumn 31, Issue 1, 2016, Pages 24-33

  Du, Ye ^a   Li, Meiyan ^b   Chen, Jing ^a   Duan, Yonggang ^a   Wang, Xuebin ^b   Qiu, Yong ^b   Cai, Zhiming ^a   Gui, Yaoting ^a   Jiang, Hui ^b  

^a PEKING UNIVERSITY SHENZHEN HOSPITAL   (China)

^b BGI SHENZHEN   (China)

Author keywords

Asthenozoospermia; DNA methylation; Low motile sperm; Potential clinical markers; Promoter targeted bisulfite sequencing

Indexed keywords

ACTIN GAMMA ENTERIC SMOOTH MUSCLE; ALPHA TUBULIN; ALPHA TUBULIN 3D; BISULFITE; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 16; DNAJ HOMOLOG SUBFAMILY MEMBER 13; G ANTIGEN 12D; G ANTIGEN 2B; GENOMIC DNA; IDITOL DEHYDROGENASE; INTRAFLAGELLAR TRANSPORT PROTEIN 122 HOMOLOG; MELANOMA ANTIGEN FAMILY B 10; OVOCHYMASE 2; PROLACTIN RECEPTOR; PROTEIN; SPERM ASSOCIATED ANTIGEN 1; SPERMATOGENESIS ASSOCIATED SERINE RICH 2; T COMPLEX ASSOCIATED TESTIS EXPRESSED 3; TRIPARTITE MOTIF PROTEIN 64; TRIPARTITE MOTIF PROTEIN 64B; UNCLASSIFIED DRUG; HYDROGEN SULFITE; SULFITE;

ADULT; ARTICLE; ASTHENOSPERMIA; CASE CONTROL STUDY; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CPG ISLAND; DNA ISOLATION; DNA LIBRARY; DNA METHYLATION; DNA SEQUENCE; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; LIQUID HYBRIDIZATION CAPTURE BASED BISULFITE SEQUENCING; MALE; MOLECULAR PATHOLOGY; NUCLEOTIDE SEQUENCE; SPERMATOGENESIS; SPERMATOZOON MOTILITY; GENETICS; METABOLISM; PROCEDURES; PROMOTER REGION;

ADULT; ASTHENOZOOSPERMIA; CASE-CONTROL STUDIES; DNA METHYLATION; HUMANS; MALE; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SPERM MOTILITY; SPERMATOGENESIS; SULFITES;

EID: 84957604462     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dev283     Document Type: Article

References (63)

1. Aoki VW, Emery BR, Carrell DT. Global sperm deoxyribonucleic acid methylation is unaffected in protamine-deficient infertile males. Fertil Steril 2006;86:1541-1543.
2. Aston KI, Carrell DT. Genome-wide study of single-nucleotide polymorphisms associated with azoospermia and severe oligozoospermia. J Androl 2009;30:711-725.
3. Aston KI, Punj V, Liu L, Carrell DT. Genome-wide sperm deoxyribonucleic acid methylation is altered in some men with abnormal chromatin packaging or poor in vitro fertilization embryogenesis. Fertil Steril 2012;97:285-292.
4. Barrow TM, Michels KB. Epigenetic epidemiology of cancer. Biochem Biophys Res Commun 2014;455:70-83.
5. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK. DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 2011;12:R10.
6. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, Niveleau A, Guerin JF. Influence of global sperm DNA methylation on IVF results. Hum Reprod 2005;20:768-773.
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. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 2009;180:462-467.
10. Cao W, Aghajanian HK, Haig-Ladewig LA, Gerton GL. Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase. Biol Reprod 2009;80:124-133.
11. Chen J, Wang Y, Wei B, Lai Y, Yan Q, Gui Y, Cai Z. Functional expression of ropporin in human testis and ejaculated spermatozoa. J Androl 2011;32:26-32.
12. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, Nelson HH, Karagas MR, Padbury JF, Bueno R et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 2009;5:e1000602.
13. Clevenger CV, Gadd SL, Zheng J. New mechanisms for PRLr action in breast cancer. Trends Endocrinol Metab 2009;20:223-229.
14. Edgar R, Mazor Y, Rinon A, Blumenthal J, Golan Y, Buzhor E, Livnat I, Ben-Ari S, Lieder I, Shitrit A et al. LifeMap Discovery: the embryonic development, stem cells, and regenerative medicine research portal. PLoS One 2013;8:e66629.
15. Eslamian G, Amirjannati N, Rashidkhani B, Sadeghi MR, Baghestani AR, Hekmatdoost A. Dietary fatty acid intakes and asthenozoospermia: a case-control study. Fertil Steril 2015;103:190-198.
16. Feinberg AP, Irizarry RA. Evolution in health and medicine Sackler colloquium: stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc Natl Acad Sci USA 2010;107(Suppl 1):1757-1764.
17. Ferfouri F, Boitrelle F, Ghout I, Albert M, Molina Gomes D, Wainer R, Bailly M, Selva J, Vialard F. A genome-wide DNA methylation study in azoospermia. Andrology 2013;1:815-821.
18. Ferlin A, Arredi B, Foresta C. Genetic causes of male infertility. Reprod Toxicol 2006;22:133-141.
19. Galeraud-Denis I, Lambard S, Carreau S. Relationship between chromatin organization, mRNAs profile and human male gamete quality. Asian J Androl 2007;9:587-592.
20. Gao F, Wang J, Ji G, Liu S, Yao Y, Wang T, Wu H, Xia Y, Gong D, Jiang H et al. Clustering of cancer cell lines using a promoter-targeted liquid hybridization capture-based bisulfite sequencing approach. Technol Cancer Res Treat 2015;14:383-394.
21. Guo J, Zhao Y, Huang W, Hu W, Gu J, Chen C, Zhou J, Peng Y, Gong M, Wang Z. Sperm motility inversely correlates with seminal leptin levels in idiopathic asthenozoospermia. Int J Clin Exp Med 2014;7:3550-3555.
22. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002;117:15-23.
23. Hammoud SS, Purwar J, Pflueger C, Cairns BR, Carrell DT. Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility. Fertil Steril 2010;94:1728-1733.
24. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, Wen B, Wu H, Liu Y, Diep D et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet 2011;43:768-775.
25. Homan GF, Davies M, Norman R. The impact of lifestyle factors on reproductive performance in the general population and those undergoing infertility treatment: a review. Hum Reprod Update 2007;13:209-223.
26. Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, Sokol RZ. Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS One 2007;2:e1289.
27. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
28. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33(Suppl):245-254.
29. Jenkins TG, Aston KI, Trost C, Farley J, Hotaling JM, Carrell DT. Intra-sample heterogeneity of sperm DNA methylation. Mol Hum Reprod 2015;21:313-319.
30. Jungwirth A, Giwercman A, Tournaye H, Diemer T, Kopa Z, Dohle G, Krausz C. European Association of Urology guidelines on Male Infertility: the 2012 update. Eur Urol 2012;62:324-332.
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.
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. Ku CS, Naidoo N, Wu M, Soong R. Studying the epigenome using next generation sequencing. J Med Genet 2011;48:721-730.
34. Kuhtz J, Schneider E, El Hajj N, Zimmermann L, Fust O, Linek B, Seufert R, Hahn T, Schorsch M, Haaf T. Epigenetic heterogeneity of developmentally important genes in human sperm: implications for assisted reproduction outcome. Epigenetics 2014;9:1648-1658.
35. Lande-Diner L, Zhang J, Ben-Porath I, Amariglio N, Keshet I, Hecht M, Azuara V, Fisher AG, Rechavi G, Cedar H. Role of DNA methylation in stable gene repression. J Biol Chem 2007;282:12194-12200.
36. Laurentino S, Beygo J, Nordhoff V, Kliesch S, Wistuba J, Borgmann J, Buiting K, Horsthemke B, Gromoll J. Epigenetic germline mosaicism in infertile men. Hum Mol Genet 2015;24:1295-1304.
37. Li W, Liu G. DNAJB13, a type II HSP40 family member, localizes to the spermatids and spermatozoa during mouse spermatogenesis. BMC Dev Biol 2014;14:38.
38. Lin W, Zhou X, Zhang M, Li Y, Miao S, Wang L, Zong S, Koide SS. Expression and function of the HSD-3.8 gene encoding a testis-specific protein. Mol Hum Reprod 2001;7:811-818.
39. Liu G, Lu GX, Xing XW. Molecular cloning of TSARG6 gene related to apoptosis in human spermatogenic cells. Acta Biochim Biophys Sin (Shanghai) 2004;36:93-98.
40. Liu N, Qiao Y, Cai C, Lin W, Zhang J, Miao S, Zong S, Koide SS, Wang L. A sperm component, HSD-3.8 (SPAG1), interacts with G-protein beta 1 subunit and activates extracellular signal-regulated kinases (ERK). Front Biosci 2006;11:1679-1689.
41. Luconi M, Forti G, Baldi E. Pathophysiology of sperm motility. Front Biosci 2006;11:1433-1447.
42. Marques CJ, Francisco T, Sousa S, Carvalho F, Barros A, Sousa M. Methylation defects of imprinted genes in human testicular spermatozoa. Fertil Steril 2010;94:585-594.
43. Mikolcevic P, Sigl R, Rauch V, Hess MW, Pfaller K, Barisic M, Pelliniemi LJ, Boesl M, Geley S. Cyclin-dependent kinase 16/PCTAIRE kinase 1 is activated by cyclin Y and is essential for spermatogenesis. Mol Cell Biol 2012;32:868-879.
44. Miller D, Briggs D, Snowden H, Hamlington J, Rollinson S, Lilford R, Krawetz SA. A complex population of RNAs exists in human ejaculate spermatozoa: implications for understanding molecular aspects of spermiogenesis. Gene 1999;237:385-392.
45. Montjean D, Zini A, Ravel C, Belloc S, Dalleac A, Copin H, Boyer P, McElreavey K, Benkhalifa M. Sperm global DNA methylation level: association with semen parameters and genome integrity. Andrology 2015;3:235-240.
46. Murrell A, Heeson S, Cooper WN, Douglas E, Apostolidou S, Moore GE, Maher ER, Reik W. An association between variants in the IGF2 gene and Beckwith-Wiedemann syndrome: interaction between genotype and epigenotype. Hum Mol Genet 2004;13:247-255.
47. Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, Goncalves J, Plancha CE. Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 2010;25:2647-2654.
48. Neesen J, Drenckhahn JD, Tiede S, Burfeind P, Grzmil M, Konietzko J, Dixkens C, Kreutzberger J, Laccone F, Omran H. Identification of the human ortholog of the t-complex-encoded protein TCTE3 and evaluation as a candidate gene for primary ciliary dyskinesia. Cytogenet Genome Res 2002;98:38-44.
49. Pacheco SE, Houseman EA, Christensen BC, Marsit CJ, Kelsey KT, Sigman M, Boekelheide K. Integrative DNA methylation and gene expression analyses identify DNA packaging and epigenetic regulatory genes associated with low motility sperm. PLoS One 2011;6:e20280.
50. Poplinski A, Tuttelmann F, Kanber D, Horsthemke B, Gromoll J. Idiopathic male infertility is strongly associated with aberrant methylation of MEST and IGF2/H19 ICR1. Int J Androl 2010;33:642-649.
51. Pujianto DA, Curry BJ, Aitken RJ. Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation. Endocrinology 2010;151:1269-1279.
52. Salvolini E, Buldreghini E, Lucarini G, Vignini A, Lenzi A, Di Primio R, Balercia G. Involvement of sperm plasma membrane and cytoskeletal proteins in human male infertility. Fertil Steril 2013;99:697-704.
53. Sato A, Hiura H, Okae H, Miyauchi N, Abe Y, Utsunomiya T, Yaegashi N, Arima T. Assessing loss of imprint methylation in sperm from subfertile men using novel methylation polymerase chain reaction Luminex analysis. Fertil Steril 2011;95:129-134, 134 e121-124.
54. Senoo M, Hoshino S, Mochida N, Matsumura Y, Habu S. Identification of a novel protein p59(scr), which is expressed at specific stages of mouse spermatogenesis. Biochem Biophys Res Commun 2002;292:992-998.
55. Siffroi JP, Dadoune JP. Accumulation of transcripts in the mature human sperm nucleus: implication of the haploid genome in a functional role. Ital J Anat Embryol 2001;106:189-197.
56. Sousa AP, Amaral A, Baptista M, Tavares R, Caballero Campo P, Caballero Peregrin P, Freitas A, Paiva A, Almeida-Santos T, Ramalho-Santos J. Not all sperm are equal: functional mitochondria characterize a subpopulation of human sperm with better fertilization potential. PLoS One 2011;6:e18112.
57. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008;9:465-476.
58. Urdinguio RG, Bayon GF, Dmitrijeva M, Torano EG, Bravo C, Fraga MF, Bassas L, Larriba S, Fernandez AF. Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod 2015;30:1014-1028.
59. Wu W, Shen O, Qin Y, Niu X, Lu C, Xia Y, Song L, Wang S, Wang X. Idiopathic male infertility is strongly associated with aberrant promoter methylation of methylenetetrahydrofolate reductase (MTHFR). PLoS One 2010;5:e13884.
60. Xi Y, Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 2009;10:232.
61. Zhang ML, Wang LF, Miao SY, Koide SS. Isolation and sequencing of the cDNA encoding the 75-kD human sperm protein related to infertility. Chin Med J (Engl) 1992;105:998-1003.
62. Zogel C, Bohringer S, Gross S, Varon R, Buiting K, Horsthemke B. Identification of cis- and trans-acting factors possibly modifying the risk of epimutations on chromosome 15. Eur J Hum Genet 2006;14:752-758.
63. Zorrilla M, Yatsenko AN. The genetics of infertility: current status of the field. Curr Genet Med Rep 2013;1.