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:: Volume 31, Issue 1 (spring 2021) ::
MEDICAL SCIENCES 2021, 31(1): 1-13 Back to browse issues page
The role and importance of DNA methylation in spermatogenesis process
Arezou Nematollahi1 , MSc, Department of Animal Biotechnology, Reproductive Biomedicine Research Center, Royan Institute f Tavalaee 2, Atefeh Rezaeian1 , Mohammad Hossein Nasr- Esfahani3
1- MSc, Department of Animal Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran
2- Associate Professor, Department of Animal Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran , m.tavalaee@royan-rc.ac.ir
3- Professor, Department of Animal Biotechnology, Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran . Embryologist, Isfahan Fertility and Infertility Center, Isfahan, Iran
Abstract:   (2374 Views)
Background: DNA methylation is one of the epigenetic marks that are created by de novo DNA methylation and be maintained through cell division. This process is catalyzed by DNA methyltransferases. DNA methylation establishment in germ line is important, since they have the potential to regulate gene expression in offspring and improper DNA methylation patterns in germ lines has serious consequences on development post fertilization. Dysregulation in epigenetic changes, especially sperm DNA methylation, may play an important role in the development of numerous diseases and has a negative effect on male fertility. The aim of this review study was to discuss about DNA methylation process and enzymes involved in this procedure and also the impact of environmental factors on the spermatogenesis process.
Materials and methods: A search was conducted according to keywords in databases such as Scopus, PubMed and Google Scholar. Then, all articles that met the inclusion criteria, between 1975 and 2017, were examined.
Results: Disorders in expression of DNA methyltransferases increase cellular oxidative stress and lifestyle can affect DNA methylation patterns during spermatogenesis and fertility potential in men.
Conclusion: As sperm DNA methylation is closely related to male infertility, it is important to understand underlying DNA methylation mechanisms in order to develop therapeutic strategies
Keywords: Epigenetic, DNA methylation, Spermatogenesis, Male infertility.
Full-Text [PDF 478 kb]   (3964 Downloads)    
Semi-pilot: Systematic Review | Subject: Genetic
Received: 2020/01/7 | Accepted: 2020/09/3 | Published: 2021/03/24
References
1. Waddington CH, Ed. The Evolution of an Evolutionist. Ithaca, NY: Cornell University Press; 1975.
2. Liyanage VR, Jarmasz JS, Murugeshan N, Del Bigio MR, Rastegar M, Davie JR. DNA modifications function and applications in normal and disease States. Biology (Basel) 2014; 3: 670 -723. [DOI:10.3390/biology3040670] [PMID] [PMCID]
3. Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2010; 2:657-69. [DOI:10.2217/epi.10.44] [PMID] [PMCID]
4. Schagdarsurengin U, Steger K. Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat Rev Urol 2016; 13: 584-95. [DOI:10.1038/nrurol.2016.157] [PMID]
5. Stuppia L, Franzago M, Ballerini P, Gatta V, Antonucci I. Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics 2015; 7:120. [DOI:10.1186/s13148-015-0155-4] [PMID] [PMCID]
6. Boissonnas CC, Jouannet P, Jammes H. Epigenetic disorders and male subfertility. Fertil Steril 2013; 99: 624-31. [DOI:10.1016/j.fertnstert.2013.01.124] [PMID]
7. Razin A, Riggs AD. DNA methylation and gene function. Science 1980; 210: 604-10. [DOI:10.1126/science.6254144] [PMID]
8. Yuan HF, Zhao K, Zang Y, Liu CY, Hu ZY, Wei JJ, et al. Effect of folate deficiency on promoter methylation and gene expression of Esr1, Cav1, and Elavl1, and its influence on spermatogenesis. Oncotarget 2017; 8: 24130-141. [DOI:10.18632/oncotarget.15731] [PMID] [PMCID]
9. Uysal F, Akkoyunlu G, Ozturk S. DNA methyltransferases exhibit dynamic expression during spermatogenesis. Reprod Biomed Online 2016; 33:690-702. [DOI:10.1016/j.rbmo.2016.08.022] [PMID]
10. Jin B, Li Y, Robertson KD. DNA methylation: superior or subordinate in the epigenetic hierarchy. Genes Cancer 2011; 2:607-17. [DOI:10.1177/1947601910393957] [PMID] [PMCID]
11. Moison C, Guieysse-Peugeot AL, Arimondo PB. DNA methylation in cancer. Atlas Genet Cytogenet Oncol Haematol 2014; 18: 285-92. [DOI:10.4267/2042/53543]
12. Sun X, St John JC. The role of the mtDNA set point in differentiation, development and tumorigenesis. Biochem J 2016; 473: 2955-71. [DOI:10.1042/BCJ20160008] [PMID]
13. Schaevitz LR, Picker JD, Rana J, Kolodny NH, Shane B, Berger-Sweeney JE, et al. Glutamate carboxypeptidase II and folate deficiencies result in reciprocal protection against cognitive and social deficits in mice: implications for neurodevelopmental disorders. Dev Neurobiol 2012; 72:891-905. [DOI:10.1002/dneu.21000] [PMID] [PMCID]
14. Kohli RM, Zhang Y. TET enzymes, TDG and the dynamics of DNA demethylation. Nature 2013; 502: 472-9. [DOI:10.1038/nature12750] [PMID] [PMCID]
15. Tan L, Shi YG. Tet family proteins and 5-hydroxymethylcytosine in development and disease. Development 2012; 139:1895-902. [DOI:10.1242/dev.070771] [PMID] [PMCID]
16. Williams K, Christensen J, Helin K. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep 2012; 13: 28-35.‌ [DOI:10.1038/embor.2011.233] [PMID] [PMCID]
17. Branco MR, Ficz G, Reik W. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 2012; 13:7-13. [DOI:10.1038/nrg3080] [PMID]
18. Aoki VW, Emery BR, Carrell DT. Global sperm deoxyribonucleic acid methylation is unaffected in protamine-deficient infertile males. Fertil Steril 2006; 86:1541 -3. [DOI:10.1016/j.fertnstert.2006.04.023] [PMID]
19. Tavalaee M, Razavi S, Nasr-Esfahani MH. Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril 2009; 91:1119-1126. [DOI:10.1016/j.fertnstert.2008.01.063] [PMID]
20. Trasler JM, Hake LE, Johnson PA, Alcivar AA, Millette CF, Hecht NB.DNA methylation and demethylation events during meiotic prophase in the mouse testis. Mol Cell Biol 1990; 10:1828 -34. [DOI:10.1128/MCB.10.4.1828] [PMID] [PMCID]
21. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T. Embryogenesis: demethylation of the zygotic paternal genome. Nature 2000; 403:501-502. [DOI:10.1038/35000656] [PMID]
22. 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. [DOI:10.1016/j.fertnstert.2009.09.010] [PMID]
23. Sonnack V, Failing K, Bergmann M, Steger, K. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 2002; 34:384-90. [DOI:10.1046/j.1439-0272.2002.00524.x] [PMID]
24. Ni K, Dansranjavin T, Rogenhofer N, Oeztuerk N, Deuker J, Bergmann M, et al. TET enzymes are successively expressed during human spermatogenesis and their expression level is pivotal for male fertility. Hum Reprod 2016; 31:1411-24. [DOI:10.1093/humrep/dew096] [PMID]
25. Potok ME, Nix DA, Parnell TJ, Cairns BR. Reprogramming the Maternal Zebrafish Genome after Fertilization to Match the Paternal Methylation Pattern. Cell 2013; 153:759-72. [DOI:10.1016/j.cell.2013.04.030] [PMID] [PMCID]
26. Molaro A, Hodges E, Fang F, Song Q, Mc Combie WR, Hannon G.J, et al. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 2011; 146:1029-41. [DOI:10.1016/j.cell.2011.08.016] [PMID] [PMCID]
27. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001;293:1089-93. [DOI:10.1126/science.1063443] [PMID]
28. Kagiwada S, Kurimoto K, Hirota T, Yamaji M, Saitou M. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J 2013; 32:340-53. [DOI:10.1038/emboj.2012.331] [PMID] [PMCID]
29. Smith ZD, Chan MM, Humm KC, Karnik R, Mekhoubad S, Regev A, et al. DNA methylation dynamics of the human preimplantation embryo. Nature 2014; 511:611-5. [DOI:10.1038/nature13581] [PMID] [PMCID]
30. 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. [DOI:10.1371/journal.pone.0001289] [PMID] [PMCID]
31. Tavalaee M, Bahreinian M, Barekat F, Abbasi H, Nasr-Esfahani, M.H. Effect of varicocelectomy on sperm functional characteristics and DNA methylation. Andrologia J 2014; 47:904-9. [DOI:10.1111/and.12345] [PMID]
32. Bahreinian M, Tavalaee M, Abbasi H, Kiani-Esfahani A, Shiravi AH, Nasr-Esfahani MH. DNA hypomethylation predisposes sperm to DNA damage in individuals with varicocele. Syst Biol Reprod Med 2015; 61:179-186. [DOI:10.3109/19396368.2015.1020116] [PMID]
33. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, iveleau A, et al. Influence of global sperm DNA methylation on IVF results. Hum Reprod 2005; 20:768-73. [DOI:10.1093/humrep/deh684] [PMID]
34. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 2007; 16:2542-51. [DOI:10.1093/hmg/ddm187] [PMID]
35. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A, et al. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 2008; 14:67-74. [DOI:10.1093/molehr/gam093] [PMID]
36. 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. [DOI:10.1530/REP-11-0008] [PMID]
37. Pacheco SE, Houseman EA, Christensen BC, Marsit CJ, Kelsey KT, Sigman, M, et al. Integrative DNA methylation and gene expression analyses identify DNA packaging and epigenetic regulatory genes associated with low motility sperm. PLoS One 2011; 6:e20280. [DOI:10.1371/journal.pone.0020280] [PMID] [PMCID]
38. Marques CJ, Joao Pinho M, Carvalho F, Bieche I, Barros A, Sousa M. DNA methylation imprinting marks and DNA methyltransferase expression in human spermatogenic cell stages. Epigenetics 2011; 6:1354-61. [DOI:10.4161/epi.6.11.17993] [PMID]
39. Urdinguio RG, Bayon GF, Dmitrijeva M, Torano EG, Bravo C, Fraga MF, et al. Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod 2015; 30:1014-28. [DOI:10.1093/humrep/dev053] [PMID]
40. Eskandari N, Tavalaee M, Zohrabi D, Nasr-Esfahani MH. Association between total globozoospermia and sperm chromatin defects. Andrologia 2018;50. [DOI:10.1111/and.12843] [PMID]
41. Aghajanpour S, Ghaedi K, Salamian A, Deemeh MR, Tavalaee M, Moshtaghian J, et al. Quantitative expression of phospholipase C zeta, as an index to assess fertilization potential of a semen sample. Hum Reprod 2011; 26:2950-2956. [DOI:10.1093/humrep/der285] [PMID]
42. Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun 2013; 4: 2889. [DOI:10.1038/ncomms3889] [PMID] [PMCID]
43. Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 2014; 345:1255903. [DOI:10.1126/science.1255903] [PMID] [PMCID]
44. Takumi S, Okamura K, Yanagisawa H, Sano T, Kobayashi Y, Nohara K. The effect of a methyl-deficient diet on the global DNA methylation and the DNA methylation regulatory pathways. J Appl Toxicol 2015; 35:1550-6. [DOI:10.1002/jat.3117] [PMID]
45. Eustache F, Mondon F, Mondon MC, Lesaffre C, Fulla Y, Berges R, et al. Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility. Environ Health Perspect 2009; 117:1272-9. [DOI:10.1289/ehp.0800158] [PMID] [PMCID]
46. Mejos KK, Kim HW, Lim EM, Chang N. Effects of parental folate deficiency on the folate content, global DNA methylation, and expressions of FRα, IGF 2 and IGF 1R in the postnatal rat liver. Nutr Res Pract 2013; 7:281-6. [DOI:10.4162/nrp.2013.7.4.281] [PMID] [PMCID]
47. Campbell JM, Lane M, Owens JA, Bakos HW. Paternal obesity negatively affects male fertility and assisted reproductive outcomes: a systematic review and meta-analysis. Reprod Biomed Online 2015; 31:593-604. [DOI:10.1016/j.rbmo.2015.07.012] [PMID]
48. Fullston T, Palmer NO, Owens JA, Mitchell M, Bakos HW, Lane M. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod 2012; 27:1391-400. [DOI:10.1093/humrep/des030] [PMID]
49. Palmer NO, Fullston T, Mitchell M, Setchell BP, Lane M. SIRT6 in mouse spermatogenesis is modulated by diet-induced obesity. Reprod Fertil Dev 2011; 23: 929-39. [DOI:10.1071/RD10326] [PMID]
50. Xu W, Fang P, Zhu Z, Dai J, Nie D, Chen Z, et al. Cigarette smoking exposure alters pebp1 DNA methylation and protein profile involved in MAPK signaling pathway in mice testis. Biol Reprod 2013; 89:142. [DOI:10.1095/biolreprod.113.111245] [PMID]
51. Dattilo M, Giuseppe D, Ettore C, Ménézo Y. Improvement of gamete quality by stimulating and feeding the endogenous antioxidant system: mechanisms, clinical results, insights on gene-environment interactions and the role of diet. J Assist Reprod Genet 2016; 33:1633-48. [DOI:10.1007/s10815-016-0767-4] [PMID] [PMCID]
52. Rose NR, Klose RJ. Understanding the relationship between DNA methylation and histone lysine methylation. Biochim Biophys 2014; 1839:1362-72. [DOI:10.1016/j.bbagrm.2014.02.007] [PMID] [PMCID]
53. Chan RC, Severson AF, Meyer BJ. Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol 2004; 167: 613-625. [DOI:10.1083/jcb.200408061] [PMID] [PMCID]
54. Kitamura A, Miyauchi N, Hamada H, Hiura H, Chiba H, Okae H, et al. Epigenetic alterations in sperm associated with male infertility. Congenit Anom (Kyoto) 2015; 55:133-144. [DOI:10.1111/cga.12113] [PMID]
55. Ghosh J, Coutifaris C, Sapienza C, Mainigi M. Global DNA methylation levels are altered by modifiable clinical manipulations in assisted reproductive technologies. Clin Epigenetics 2017; 9:14. [DOI:10.1186/s13148-017-0318-6] [PMID] [PMCID]
56. Sato A, Otsu E, Negishi H, Utsunomiya T, Arima T. Aberrant DNA methylation of imprinted loci in superovulated oocytes. Hum Reprod 2007; 22:26-35. [DOI:10.1093/humrep/del316] [PMID]
57. Chiba H, Hiura H, Okae H, Miyauchi N, Sato F, Sato A, et al. DNA methylation errors in imprinting disorders and assisted reproductive technology. Pediatr Int 2013; 55:542-9. [DOI:10.1111/ped.12185] [PMID]
58. Khosla S, Dean W, Brown D, Reik W, Feil R. Culture of preimplantation mouse embryos affects fetal development and the expression of imprinted genes. Biol Reprod 2001; 64:918-26. [DOI:10.1095/biolreprod64.3.918] [PMID]
59. Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet 2003; 361:1975-7. [DOI:10.1016/S0140-6736(03)13592-1]
60. Castillo-Fernandez JE, Loke YJ, Bass-Stringer S, Gao F, Xia Y, Wu H, et al. DNA methylation changes at infertility genes in newborn twins conceived by in vitro fertilisation. Genome Med 2017; 9:28. [DOI:10.1186/s13073-017-0413-5] [PMID] [PMCID]
61. Chen M, Norman RJ, Heilbronn LK. Does in vitro fertilisation increase type 2 diabetes and cardiovascular risk? Curr Diabetes Rev 2011; 7:426-32. [DOI:10.2174/157339911797579151] [PMID]
62. Deemeh MR, Tavalaee M, Nasr-Esfahani MH. Health of children born through artificial oocyte activation: a pilot study. Reprod Sci 2015; 22:322-8. [DOI:10.1177/1933719114542017] [PMID]
63. Sharma R, Biedenharn KR, Fedor JM, Agarwal A. Lifestyle factors and reproductive health: taking control of your fertility. Reprod Biol Endocrinol 2013; 11:66. [DOI:10.1186/1477-7827-11-66] [PMID] [PMCID]
64. Smith R, Kaune H, Parodi D, Madariaga M, Rios R, Morales I. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod 2006; 21:986-93. [DOI:10.1093/humrep/dei429] [PMID]
65. Tunc O, Tremellen K. Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 2009; 26:537-44. [DOI:10.1007/s10815-009-9346-2] [PMID] [PMCID]
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Nematollahi A, Tavalaee M D O A B R B R C R I F, Rezaeian A, Nasr- Esfahani M H. The role and importance of DNA methylation in spermatogenesis process. MEDICAL SCIENCES 2021; 31 (1) :1-13
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Volume 31, Issue 1 (spring 2021) Back to browse issues page
فصلنامه علوم پزشکی دانشگاه آزاد اسلامی واحد پزشکی تهران Medical Science Journal of Islamic Azad Univesity - Tehran Medical Branch
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