Epigenetic heterogeneity of developmentally important genes in human sperm: Implications for assisted reproduction outcome

Epigenetics

Volumn 9, Issue 12, 2014, Pages 1648-1658

  Kuhtz, Juliane ^a   Schneider, Eberhard ^a   El Hajj, Nady ^a   Zimmermann, Lena ^a   Fust, Olga ^a   Linek, Bartosz ^b   Seufert, Rudolf ^b   Hahn, Thomas ^c   Schorsch, Martin ^c   Haaf, Thomas ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c Fertility Center   (Germany)

Author keywords

ART outcome; Deep bisulfite sequencing; Epigenetic heterogeneity; GTL2; ICSI; IMSI; Sperm DNA methylation

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; PEPTIDES AND PROTEINS; PROTEIN BOLL; PROTEIN CATSPER1; PROTEIN GTL2; PROTEIN LIT1; PROTEIN PEG3; PROTEIN SNRPN; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; BOLL PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; HYDROGEN SULFITE; KCNQ1OT1 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; LONG UNTRANSLATED RNA; MEG3 NON-CODING RNA, HUMAN; NANOG PROTEIN, HUMAN; PEG3 PROTEIN, HUMAN; POU5F1 PROTEIN, HUMAN; RNA BINDING PROTEIN; SULFITE; VOLTAGE GATED POTASSIUM CHANNEL;

ALLELE; ARTICLE; DEVELOPMENTAL GENE; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC HETEROGENEITY; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; LIMITING DILUTION BISULFITE PYROSEQUENCING; MAJOR CLINICAL STUDY; MALE; MALE INFERTILITY; NORMOZOOSPERMIA; OLIGOASTHENOTERATOZOOSPERMIA; POLYMERASE CHAIN REACTION; PYROSEQUENCING; SEMEN ANALYSIS; SPERM; ASTHENOSPERMIA; CPG ISLAND; GENETIC EPIGENESIS; GENETICS; GENOME IMPRINTING; HIGH THROUGHPUT SEQUENCING; PHYSIOLOGY; PROCEDURES; REFERENCE VALUE; SINGLE CELL ANALYSIS; SPERMATOGENESIS; SPERMATOZOON;

ASTHENOZOOSPERMIA; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENOMIC IMPRINTING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOMEODOMAIN PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; OCTAMER TRANSCRIPTION FACTOR-3; POTASSIUM CHANNELS, VOLTAGE-GATED; REFERENCE VALUES; RNA, LONG NONCODING; RNA-BINDING PROTEINS; SINGLE-CELL ANALYSIS; SPERMATOGENESIS; SPERMATOZOA; SULFITES;

EID: 84922021677     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/15592294.2014.988063     Document Type: Article

References (41)

1. Singh K, Jaiswal D. Human male infertility: a complex multifactorial phenotype. Reprod Sci 2011; 18:418-25; PMID:21421900; http://dx.doi.org/10.1177/ 1933719111398148
2. Tüttelmann F, Werny F, Cooper TG, Kliesch S, Simoni M, Nieschlag E. Clinical experience with azoospermia: aetiology and chances for spermatozoa detection upon biopsy. Int J Androl 2011; 34:291-8; PMID:20609027; http://dx.doi.org/10.1111/j.1365- 2605.2010.01087.x
3. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, Gudjonsson SA, Sigurdsson A, Jonasdottir A, Jonasdottir A, et al. Rate of de novo mutations and the importance of father's age to disease risk. Nature 2012; 488:471-5; PMID:22914163; http://dx. doi.org/10.1038/nature11396
4. Bennett-Baker PE, Wilkowski J, Burke DT. Age-associated activation of epigenetically repressed genes in the mouse. Genetics 2003; 165:2055-62; PMID:14704185
5. Goyal R, Reinhardt R, Jeltsch A. Accuracy of DNA methylation pattern preservation by the Dnmt1 methyltransferase. Nucleic Acids Res 2006; 34:1182-88; PMID:16500889; http://dx.doi.org/10.1093/nar/ gkl002
6. 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; PMID:12204247; http://dx.doi.org/ 10.1016/S0925-4773(02)00181-8
7. Allegrucci C, Thurston A, Lucas E, Young L. Epigenetics and the germline. Reproduction 2005; 129:137- 49; PMID:15695608; http://dx.doi.org/10.1530/ rep.1.00360
8. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev Biol 2007; 307:368-79; PMID:17559830; http:// dx.doi.org/10.1016/j.ydbio.2007.05.002
9. Boyano MD, Andollo N, Zalduendo MM, Aréchaga J. Imprinting of mammalian male gametes is gene specific and does not occur at a single stage of differentiation. Int J Dev Biol 2008; 52:1105-11; PMID:18956343; http://dx.doi.org/10.1387/ijdb.072284mb
10. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293:1089- 93; PMID:11498579; http://dx.doi.org/10.1126/ science.1063443
11. Haaf T. Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. Curr Top Microbiol Immunol 2006; 310:13-22; PMID:16909904
12. Kelsey G. Genomic imprinting - roles and regulation in development. Endocr Dev 2007; 12:99-112; PMID:17923773
13. Carrell DT. Epigenetics of the male gamete. Fertil Steril 2012; 97:267-74; PMID:22289286; http://dx. doi.org/10.1016/j.fertnstert.2011.12.036
14. Boissonnas CC, Jouannet P, Jammes H. Epigenetic disorders and male subfertility. Fertil Steril 2013; 99:624- 31; PMID:23714437; http://dx.doi.org/10.1016/j. fertnstert.2013.01.124
15. 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; 14:67-74; PMID:18178607; http://dx.doi.org/10.1093/molehr/ gam093
16. 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; 94:1728-33; PMID:19880108; http://dx. doi.org/10.1016/j.fertnstert.2009.09.010
17. Poplinski A, Tüttelmann 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; 33:642-9; PMID:19878521
18. 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; 95:129-34; PMID:20655520; http://dx.doi.org/10.1016/j. fertnstert.2010.06.076
19. Kobayashi H, Hiura H, John RM, Sato A, Otsu E, Kobayashi N, Suzuki R, Suzuki F, Hayashi C, Utsunomiya T, et al. DNA methylation errors at imprinted loci after assisted conception originate in the parental sperm. Eur J Hum Genet 2009; 17:1582-91; PMID:19471309; http://dx.doi.org/10.1038/ ejhg.2009.68
20. 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; 5:60-9; PMID:21293114; http://dx.doi.org/10.1159/ 000323806
21. 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 2011; 97:285-92; PMID:22154369; http://dx.doi.org/ 10.1016/j.fertnstert.2011.11.008
22. 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; PMID:21674046; http://dx.doi.org/10.1371/ journal.pone.0020280
23. Schütte B, El Hajj N, Kuhtz J, Nanda I, Gromoll J, Hahn T, Dittrich M, Schorsch M, Müller T, Haaf T. Broad DNA methylation changes of spermatogenesis, inflammation and immune response-related genes in a subgroup of sperm samples for assisted reproduction. Andrology 2013; 1:822-9; PMID:23996961; http://dx. doi.org/10.1111/j.2047-2927.2013.00122.x
24. Jenkins TG, Aston KI, Pflueger C, Cairns BR, Carrell DT. Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLoS Genet 2014; 10:e1004458; PMID:25010591; http://dx.doi.org/10.1371/journal. pgen.1004458
25. Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M, Schübeler D. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 2007; 39:457- 66; PMID:17334365; http://dx.doi.org/10.1038/ ng1990
26. El Hajj N, Trapphoff T, Linke M, May A, Hansmann T, Kuhtz J, Reifenberg K, Heinzmann J, Niemann H, Daser A, et al. Limiting dilution bisulfite (pyro) sequencing reveals parent-specific methylation patterns in single early mouse embryos and bovine oocytes. Epigenetics 2011; 6:1176-88; PMID:21937882; http://dx. doi.org/10.4161/epi.6.10.17202
27. Minor A, Chow V, Ma S. Aberrant DNA methylation at imprinted genes in testicular sperm retrieved from men with obstructive azoospermia and undergoing vasectomy reversal. Reproduction 2011; 141:749-57; PMID:21389080; http://dx.doi.org/10.1530/REP-11- 0008
28. Bartoov B, Berkovitz A, Eltes F. Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med 2001; 345:1067-8; PMID:11586970; http://dx.doi.org/10.1056/NEJM200110043451416
29. Beygo J, Ammerpohl O, Gritzan D, Heitmann M, Rademacher K, Richter J, Caliebe A, Siebert R, Horsthemke B, Buiting K. Deep bisulfite sequencing of aberrantly methylated loci in a patient with multiple methylation defects. PLoS One 2013; 8:e76953; PMID:24130816; http://dx.doi.org/10.1371/journal. pone.0076953
30. Watanabe S, Tanaka A, Fujii S, Mizunuma H, Fukui A, Fukuhara R, Nakamura R, Yamada K, Tanaka I, Awata S, et al. An investigation of the potential effect of vacuoles in human sperm on DNA damage using a chromosome assay and the TUNEL assay. Hum Reprod 2011; 26:978-86; PMID:21362682; http://dx. doi.org/10.1093/humrep/der047
31. Franco JG Jr, Mauri AL, Petersen CG, Massaro FC, Silva LF, Felipe V, Cavagna M, Pontes A, Baruffi RL, Oliveira JB, et al. Large nuclear vacuoles are indicative of abnormal chromatin packaging in human spermatozoa. Int J Androl 2012; 35:46-51; PMID:21535011; http://dx.doi.org/10.1111/j.1365-2605.2011.01154.x
32. Perdrix A, Rives N. Motile sperm organelle morphology examination (MSOME) and sperm head vacuoles: state of the ART in 2013. Hum Reprod Update 2013; 19:527-41; PMID:23825157; http://dx.doi.org/ 10.1093/humupd/dmt021
33. Bartoov B, Berkovitz A, Eltes F, Kogosovsky A, Yagoda A, Lederman H, Artzi S, Gross M, Barak Y. Pregnancy rates are higher with intracytoplasmic morphologically selected sperm injection than with conventional intracytoplasmic injection. Fertil Steril 2003; 80:1413-39; PMID:14667877; http://dx.doi.org/10.1016/j. fertnstert.2003.05.016
34. Berkovitz A, Eltes F, Yaari S, Katz N, Barr I, Fishman A, Bartoov B. The morphological normalcy of the sperm nucleus and pregnancy rate of intracytoplasmic injection with morphologically selected sperm. Hum Reprod 2005; 20 185-90; PMID:15471930; http://dx. doi.org/10.1093/humrep/deh545
35. Antinori M, Licata E, Dani G, Cerusico F, Versaci C, D'Angelo D, Antinori S. Intracytoplasmic morphologically selected sperm injection: a prospective randomized trial. Reprod Biomed Online 2008; 16:835-41; PMID:18549694; http://dx.doi.org/10.1016/S1472- 6483(10)60150-2
36. Teixeira DM, Barbosa MA, Ferriani RA, Navarro PA, Raine-Fenning N, Nastri CO, Martins WP. Regular (ICSI) vs. ultra-high magnification (IMSI) sperm selection for assisted reproduction. Cochrane Database Syst Rev 2013; 7:CD010167; PMID:23884963; http://dx. doi.org/10.1002/14651858.CD010167
37. 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 2014; Epub ahead of print: PMID:25336341
38. World Health Organization. WHO Laboratory Manual for the Examination and Processing of Human Semen. 5th edition. WHO press 2010
39. Ubaldi F, Rienzi L. Morphological selection of gametes. Placenta 2008; 29 Suppl B:115-20; PMID:18762336; http://dx.doi.org/10.1016/j. placenta.2008.08.009
40. Rahmann S, Beygo J, Kanber D, Martin M, Horsthemke B, Buiting K. Amplikyzer: automated methylation analysis of amplicons from bisulfite flowgram sequencing. PeerJ PrePrints 2013; 1:e122v2
41. Bock C, Reither S, Mikeska T, Paulsen M, Walter J, Lengauer T. BiQ Analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing. Bioinformatics 2005; 21:4067-8; PMID:16141249; http://dx.doi.org/10.1093/ bioinformatics/bti652