Altered DNA Methylation Patterns of the H19 Differentially Methylated Region and the DAZL Gene Promoter Are Associated with Defective Human Sperm

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Li, Bo ^a   Li, Jian bo ^a   Xiao, Xi feng ^a   Ma, Ye fei ^a   Wang, Jun ^a   Liang, Xin xin ^a   Zhao, Hong xi ^a   Jiang, Feng ^a   Yao, Yuan qing ^b   Wang, Xiao hong ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; ASTHENOSPERMIA; BINDING SITE; DAZL GENE; DISEASE SEVERITY; DNA METHYLATION; EPIGENETICS; GENE; HUMAN; MAJOR CLINICAL STUDY; MALE; MALE INFERTILITY; OLIGOSPERMIA; PHENOTYPE; POLYMERASE CHAIN REACTION; PROMOTER REGION; SEMEN ANALYSIS; TRANSPOSON;

ADULT; ASTHENOZOOSPERMIA; CASE-CONTROL STUDIES; COMPARATIVE GENOMIC HYBRIDIZATION; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; OLIGOSPERMIA; PROMOTER REGIONS, GENETIC; RNA, LONG NONCODING; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 84883178618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071215     Document Type: Article

References (43)

1. Raheem AA, Ralph D, Minhas S, (2012) Male Infertility. J Clin Urology 5: 254-268.
2. Gianotten J, Lombardi MP, Zwinderman AH, Lilford RJ, van der Veen F, (2004) Idiopathic impaired spermatogenesis: genetic epidemiology is unlikely to provide a short-cut to better understanding. Hum Reprod Update 10: 533-539.
3. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, et al. (2008) Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 14: 67-74.
4. Boissonnas CC, Abdalaoui HE, Haelewyn V, Fauque P, Dupont JM, et al. (2010) Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur J Hum Genet 18: 73-80.
5. Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, et al. (2010) Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 25: 2647-2654.
6. Wu W, Shen O, Qin Y, Niu X, Lu C, et al. (2010) Idiopathic male infertility is strongly associated with aberrant promoter methylation of methylenetetrahydrofolate reductase (MTHFR). PLoS One 5: e13884.
7. Bartolomei MS, Zemel S, Tilghman SM, (1991) Parental imprinting of the mouse H19 gene. Nature 351: 153-155.
8. Zhang Y, Tycko B, (1992) Monoallelic expression of the human H19 gene. Nat Genet 1: 40-44.
9. Banerjee S, Singh PB, Rasberry C, Cattanach BM, (2000) Embryonic inheritance of the chromatin organisation of the imprinted H19 domain in mouse spermatozoa. Mech Dev 90: 217-226.
10. Poplinski A, Tüttelmann 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.
11. Arney KL, (2003) H19 and Igf2-enhancing the confusion? Trends Genet 19: 17-23.
12. Chai NN, Phillips A, Fernandez A, Yen PH, (1997) A putative human maleinfertility gene DAZLA: genomic structure and methylation status. Mol Hum Reprod 3: 705-708.
13. Yen PH, (2004) Putative biological functions of the DAZ family. Int J Androl 27: 125-129.
14. Karashima T, Sugimoto A, Yamamoto M, (2000) Caenorhabditis elegans homologue of the human azoospermia factor DAZ is required for oogenesis but not for spermatogenesis. Development 127: 1069-1079.
15. Houston DW, King ML, (2000) A critical role for Xdazl, a germ plasm-localized RNA, in the differentiation of primordial germ cells in Xenopus. Development 127: 447-456.
16. Schrans-Stassen BH, Saunders PT, Cooke HJ, de Rooij DG, (2001) Nature of the spermatogenic arrest in Dazl -/- mice. Biol Reprod 65: 771-776.
17. Lin Y, Page DC, (2005) Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev Biol 288: 309-316.
18. Vogel T, Speed RM, Ross A, Cooke HJ, (2002) Partial rescue of the Dazl knockout mouse by the human DAZLgene. Mol Hum Reprod 8: 797-804.
19. Lin YM, Chen CW, Sun HS, Tsai SJ, Hsu CC, et al. (2001) Expression patterns and transcript concentrations of the autosomal DAZL gene in testes of azoopsermic men. Mol Hum Reprod 11: 1015-1022.
20. Lin YM, Chen CW, Sun HS, Tsai SJ, Lin JS, et al. (2002) Presence of DAZL transcript and protein in mature spermatozoa. Fertil Steril 77: 626-629.
21. Teng YN, Lin YM, Sun HF, Hsu PY, Chung CL, et al. (2006) Association of DAZL haplotypes with spermatogenic failure in infertile men. Fertil Steril 86: 129-135.
22. Teng YN, Chang YP, Tseng JT, Kuo PH, Lee IW, et al. (2012) A single-nucleotide polymorphism of the DAZL gene promoter confers susceptibility to spermatogenic failure in the Taiwanese Han. Hum Reprod 27: 2857-2865.
23. Hargreave TB, McGowan B, Harvey J, McParland M, Elton RA, (1986) Is a male infertility clinic of any use? Br J Urol 58: 188-193.
24. Hwang K, Walters RC, Lipshultz LI, (2011) Contemporary concepts in the evaluation and management of male infertility. Nat Rev Urol 8: 86-94.
25. Davies MJ, Moore VM, Willson KJ, Van Essen P, Priest K, et al. (2012) Reproductive technologies and the risk of birth defects. N Engl J Med 366: 1803-1813.
26. Grønskov K, Poole RL, Hahnemann JM, Thomson J, Tümer Z, et al. (2011) Deletions and rearrangements of the H19/IGF2 enhancer region in patients with Silver-Russell syndrome and growth retardation. J Med Genet 48: 308-311.
27. Le Bouc Y, Rossignol S, Azzi S, Steunou V, Netchine I, et al. (2010) Epigenetics, genomic imprinting and assisted reproductive technology. Ann Endocrinol (Paris) 71(3): 237-238.
28. 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.
29. Suzuki JJ, Therrien J, Filion F, Lefebvre R, Goff AK, et al. (2011) Loss of methylation at H19DMD is associated with biallelic expression and reduced development in cattle derived by somatic cell nuclear transfer. Biol Reprod 84: 947-956.
30. Bjornsson HT, Cui H, Gius D, Fallin MD, Feinberg AP, (2004) The New Field Of Epigenomics: Implications for Cancer and Other Common Disease Research. Cold Spring Harb Symp Quant Biol 69: 447-456.
31. Gabory A, Ripoche MA, Le Digarcher A, Watrin F, Ziyyat A, et al. (2009) H19 acts as a trans regulator of the imprinted gene network controlling growth in mice. Development 136: 3413-3421.
32. Cooper WN, Luharia A, Evans GA, Raza H, Haire AC, et al. (2005) Molecular subtypes and phenotypic expression of Beckwith-Wiedemann syndrome. Eur J Hum Genet 13: 1025-1032.
33. Bartholdi D, Krajewska-Walasek M, Ounap K, Gaspar H, Chrzanowska KH, et al. (2009) Epigenetic mutations of the imprinted IGF2-H19 domain in Silver-Russell syndrome (SRS): results from a large cohort of patients with SRS and SRS-like phenotypes. J Med Genet 46: 192-197.
34. Netchine I, Rossignol S, Dufourg MN, Azzi S, Rousseau A, et al. (2007) 11p15 imprinting center region 1 loss of methylation is a common and specific cause of typical Russell-Silver syndrome: clinical scoring system and epigenetic- phenotypic correlations. J Clin Endocrinol Metab 92: 3148-3154.
35. Liu DY, Liu ML, Garrett C, Baker HW, (2007) Comparison of the frequency of defective sperm-zona pellucida (ZP) binding and the ZP-induced acrosome reaction between subfertile men with normal and abnormal semen. Hum Reprod 22: 1878-1884.
36. Ariel I, Sughayer M, Fellig Y, Pizov G, Ayesh S, et al. (2000) The imprinted H19 gene is a marker of early recurrence in human bladder carcinoma. Mol Pathol 53: 320-323.
37. Takai D, Gonzales FA, Tsai YC, Thayer MJ, Jones PA, (2001) Large-scale mapping of methylcytosines in CTCF-binding sites in the human H19 promoter and aberrant hypomethylation in human bladder cancer. Hum Mol Genet 10: 2619-2626.
38. van Gurp RJ, Oosterhuis JW, Kalscheuer V, Mariman EC, Looijenga LH, (1994) Biallelic expression of the H19 and IGF2 genes in human testicular germ cell tumors. J Natl Cancer Inst 86: 1070-1075.
39. Berteaux N, Aptel N, Cathala G, Genton C, Coll J, et al. (2008) Novel H19 antisense RNA overexpressed in breast cancer contributes to paternal IGF2 expression. Mol Cell Biol 28: 6731-6745.
40. Woodcock DM, Lawler CB, Linsenmeyer ME, Doherty JP, Warren WD, (1997) Asymmetric methylation in the hypermethylated CpG promoter region ofthe human L1 retrotransposon. J Biol Chem 272: 7810-7816.
41. Marques CJ, Carvalho F, Sousa M, Barros A, (2004) Genomic imprinting in disruptive spermatogenesis. Lancet 363: 1700-1726.
42. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, et al. (2005) BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 21: 4067 - 4068.
43. Al-Khtib M, Perret A, Khoueiry R, Ibala-Romdhane S, Blachère T, et al. (2011) Vitrification at the germinal vesicle stage does not affect the methylation profile of H19 and KCNQ1OT1 imprinting centers in human oocytes subsequently matured in vitro. Fertil Steril. 95: 1955-1960.