DNA hypomethylation predisposes sperm to DNA damage in individuals with varicocele

References

• Agarwal, A., Prabakaran, S. and Allamaneni, S.S. (2006) Relationship between oxidative stress, varicocele and infertility: A meta-analysis. Reprod Biomed Online 12:630–633
   PubMed Web of Science ®Google Scholar
• Aitken, R.J., De Iuliis, G.N., Finnie, J.M., Hedges, A. and McLachlan, R.I. (2010) Analysis of the relationships between oxidative stresses, DNA damage and sperm vitality in a patient population: Development of diagnostic criteria. Hum Reprod 25:2415–2426
   PubMed Web of Science ®Google Scholar
• Aoki, V.W., Emery, B.R. and Carrell, D.T. (2006) Global sperm deoxyribonucleic acid methylation is unaffected in protamine-deficient infertile males. Fertil Steril 86:1541–1543
   PubMed Web of Science ®Google Scholar
• Benchaib, M., Braun, V., Ressnikof, D., Lornage, J., Durand, P., Niveleau, A., et al. (2005) Influence of global sperm DNA methylation on IVF results. Hum Reprod 20:768–773
   PubMed Web of Science ®Google Scholar
• Borini, A., Tarozzi, N., Bizzaro, D., Bonu, M.A., Fava, L., Flamigni, C., et al. (2006) Sperm DNA fragmentation: Paternal effect on early post-implantation embryo development in ART. Hum Reprod 21:2876–2881
   PubMed Web of Science ®Google Scholar
• Dada, R., Shamsi, M.B., Venkatesh, S., Gupta, N.P. and Kumar, R. (2010) Attenuation of oxidative stress and DNA damage in varicocelectomy: Implications in infertility management. Indian J Med Res 132:728–730
   PubMed Web of Science ®Google Scholar
• Duran, E.H., Morshedi, M., Taylor, S. and Oehninger S. (2002) Sperm DNA quality predicts intrauterine insemination outcome: A prospective cohort study. Hum Reprod 17:3122–3128
   PubMed Web of Science ®Google Scholar
• Guo, F., Li, X., Liang, D., Li, T., Zhu, P., Guo, H., et al. (2014) Active and passive demethylation of male and female pronuclear DNA in the Mammalian zygote. Cell Stem Cell 15:447–458
   PubMed Web of Science ®Google Scholar
• Henkel, R.R. (2011) Leukocytes and oxidative stress: Dilemma for sperm function and male fertility. Asian J Androl 13:43–52
   PubMed Web of Science ®Google Scholar
• Kheirollahi-Kouhestani, M., Razavi, S., Tavalaee, M., Deemeh, M.R., Mardani, M., Moshtaghian, J., et al. (2009) Selection of sperm based on combined density gradient and Zeta method may improve ICSI outcome. Hum Reprod 24:2409–2416
   PubMed Web of Science ®Google Scholar
• Kiani-Esfahani, A., Tavalaee, M., Deemeh, M.R., Hamiditabar, M. and Nasr-Esfahani, M.H. (2012) DHR123: An alternative probe for assessment of ROS in human spermatozoa. Syst Biol Reprod Med 58:168–174
   PubMed Web of Science ®Google Scholar
• Kobayashi, H., Sato, A., Otsu, E., Hiura, H., Tomatsu, C., Utsunomiya, T., et al. (2007) Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 1:2542–2551
   Google Scholar
• Kobayashi, H., Sakurai, T., Imai, M., Takahashi, N., Fukuda, A., Yayoi, O., et al. (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8:e1002440
   PubMed Web of Science ®Google Scholar
• Krausz, C., Sandoval, J., Sayols, S., Chianese, C., Giachini, C., Heyn, H., et al (2012) Novel insights into DNA methylation features in spermatozoa: Stability and peculiarities. PLoS One 7(10):e44479
   PubMedGoogle Scholar
• Mayer, W., Niveleau, A., Walter, J., Fundele, R. and Haaf, T. (2000) Demethylation of the zygotic paternal genome. Nature 403:501–502
   PubMed Web of Science ®Google Scholar
• Nasr-Esfahani, M.H., Razavi, S. and Mardani, M. (2001) Relation between different human sperm nuclear maturity tests and in vitro fertilization. J Assist Reprod Genet 18:219–225
   PubMed Web of Science ®Google Scholar
• Parikh, F.R., Kamat, S.A., Kodwaney, G.G. and Balaiah, D. (1996) Computer-assisted semen analysis parameters in men with varicocele: Is surgery helpful? Fertil Steril 66:440–445
   PubMed Web of Science ®Google Scholar
• Pasqualotto, F.F., Lucon, A.M., de Góes, P.M., Sobreiro, B.P., Hallak, J., Pasqualotto, E.B., et al. (2005) Semen profile, testicular volume, and hormonal levels in infertile patients with varicoceles compared with fertile men with and without varicocele. Fertil Steril 83:74–77
   PubMed Web of Science ®Google Scholar
• Reik, W., Dean, W. and Walter, J. (2001) Epigenetic reprogramming in mammalian development. Science 293:1089–1093
   PubMed Web of Science ®Google Scholar
• Robinson, L., Gallos, I.D., Conner, S.J., Rajkhowa, M., Miller, D., Lewis, S., et al. (2012) The effect of sperm DNA fragmentation on miscarriage rates: A systematic review and meta-analysis. Hum Reprod 27:2908–2917
   PubMed Web of Science ®Google Scholar
• Sadek, A., Almohamdy, A.S., Zaki, A., Aref, M., Ibrahim, S.M. and Mostafa, T. (2011) Sperm chromatin condensation in infertile men with varicocele before and after surgical repair. Fertil Steril 95:1705–1708
   PubMed Web of Science ®Google Scholar
• Sakkas, D. and Alvarez, J.G. (2010) Sperm DNA fragmentation: Mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 93:1027–1036. Review
   PubMed Web of Science ®Google Scholar
• Santos, F., Hendrich, B., Reik, W. and Dean, W. (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172–182
   PubMed Web of Science ®Google Scholar
• Schulte, R.T., Ohl, D.A., Sigman, M. and Smith, G.D. (2010) Sperm DNA damage in male infertility: Etiologies, assays, and outcomes. J Assist Report Genet 27:3–12
   PubMed Web of Science ®Google Scholar
• Shamsi, M.B., Imam, S.N. and Dada, R. (2011) Sperm DNA integrity assays: Diagnostic and prognostic challenges and implications in management of infertility. J Assist Reprod Genet 28:1073–1085
   PubMed Web of Science ®Google Scholar
• Shen, L., Inoue, A., He, J., Liu, Y., Lu, F. and Zhang, Y. (2014) Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell 15:459–470
   PubMed Web of Science ®Google Scholar
• Singh, A. and Agarwal, A. (2011) The Role of Sperm Chromatin Integrity and DNA Damage on Male Infertility. Open Reprod Sci J 3:65–7165
   Google Scholar
• Smallwood, S.A., Tomizawa, S., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., et al. (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43:811–814
   PubMed Web of Science ®Google Scholar
• Smith, Z.D., Chan, M.M., Mikkelsen, T.S., Gu, H., Gnirke, A., Regev, A., et al. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484:339–344
   PubMed Web of Science ®Google Scholar
• Smith, Z.D., Chan, M.M., Humm, K.C., Karnik, R., Mekhoubad, S., Regev, A., et al. (2014) DNA methylation dynamics of the human preimplantation embryo. Nature 511:611–615
   PubMed Web of Science ®Google Scholar
• Tavalaee, M., Razavi, S. and Nasr-Esfahani, M.H. (2009) Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril 91:1119–1126
   PubMed Web of Science ®Google Scholar
• Tavalaee, M., Abbasi, H., Deemeh, M.R., Fotohi, F., Sadoughi Gilani, M.A. and Nasr Esfahani, M.H. (2012) Semen parameters and chromatin packaging in microsurgical varicocelectomy patients. Int J Fertil Steril 6:165–174
   Web of Science ®Google Scholar
• Tavalaee, M., Bahreinian, M., Barekat, F., Abbasi, H. and Nasr-Esfahani, M.H. (2014) Effect of varicocelectomy on sperm functional characteristics and DNA methylation. Andrologia J. 1–6. doi: 10.1111/and.12345. [Epub ahead of print]
   Google Scholar
• Tunc, O. and Tremellen, K. (2009) Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 26:537–544
   PubMed Web of Science ®Google Scholar
• Turk, P.W., Laayoun, A., Smith, S.S. and Weitzman, S.A. (1995) DNA adducts 8-hydroxyl-2′-deoxyguanosine (8hydroxyguanine) affects function of human DNA methyltransferase. Carcinogenesis 16:1253–1255
   PubMed Web of Science ®Google Scholar
• Valinluck, V., Tsai, H.H., Rogstad, D.K., Burdzy, A., Bird, A. and Sowers, L.C. (2004) Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res 32:4100–4108
   PubMed Web of Science ®Google Scholar
• Wang, Y.J., Zhang, R.Q., Lin, Y.J., Zhang, R.G. and Zhang, W.L. (2012) Relationship between varicocele and sperm DNA damage and the effect of varicocele repair: A meta-analysis. Reprod Biomed Online 25:307–314
   PubMed Web of Science ®Google Scholar
• WHO (2010) WHO laboratory manual for the examination and processing of human semen. Fifth edition, World Health Organization. WHO Press, Geneva, Switzerland
   Google Scholar
• Zini, A., Defreitas, G., Freeman, M., Hechter, S. and Jarvi, K. (2000) Varicocele is associated with abnormal retention of cytoplasmic droplets by human spermatozoa. Fertil Steril 74:461–464
   PubMed Web of Science ®Google Scholar