1,722
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Genome-Wide Methylation Analyses of Human Sperm Unravel Novel Differentially Methylated Regions in Asthenozoospermia

ORCID Icon, , ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 951-964 | Received 11 Apr 2022, Accepted 03 Aug 2022, Published online: 25 Aug 2022

References

  • Agarwal A , BaskaranS , ParekhNet al. Male infertility. Lancet397(10271), 319–333 (2021).
  • Tu C , WangW , HuT , LuG , LinG , TanYQ. Genetic underpinnings of asthenozoospermia. Best Pract. Res. Clin. Endocrinol. Metab.34(6), 101472 (2020).
  • Cooper TG , NoonanE , Von EckardsteinSet al. World Health Organization reference values for human semen characteristics. Hum. Reprod. Update16(3), 231–245 (2010).
  • Toure A , MartinezG , KherrafZEet al. The genetic architecture of morphological abnormalities of the sperm tail. Hum. Genet.140(1), 21–42 (2021).
  • Li WN , ZhuL , JiaMM , YinSL , LuGX , LiuG. Missense mutation in DNAJB13 gene correlated with male fertility in asthenozoospermia. Andrology8(2), 299–306 (2020).
  • Akbari A , PipitoneGB , AnvarZet al. ADCY10 frameshift variant leading to severe recessive asthenozoospermia and segregating with absorptive hypercalciuria. Hum. Reprod.34(6), 1155–1164 (2019).
  • Jaenisch R , BirdA. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet.33 Suppl., 245–254 (2003).
  • Bird A . DNA methylation patterns and epigenetic memory. Genes Dev.16(1), 6–21 (2002).
  • Yu B , DongX , GravinaSet al. Genome-wide, single-cell DNA methylomics reveals increased non-CpG methylation during human oocyte maturation. Stem Cell Rep.9(1), 397–407 (2017).
  • Ehrlich M , Gama-SosaMA , HuangLHet al. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res.10(8), 2709–2721 (1982).
  • Robert MF , MorinS , BeaulieuNet al. DNMT1 is required to maintain CpG methylation and aberrant gene silencing in human cancer cells. Nat. Genet.33(1), 61–65 (2003).
  • Rhee I , BachmanKE , ParkBHet al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature416(6880), 552–556 (2002).
  • Kim GD , NiJ , KelesogluN , RobertsRJ , PradhanS. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J.21(15), 4183–4195 (2002).
  • Okano M , BellDW , HaberDA , LiE. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell99(3), 247–257 (1999).
  • Chodavarapu RK , FengS , BernatavichuteYVet al. Relationship between nucleosome positioning and DNA methylation. Nature466(7304), 388–392 (2010).
  • Robertson KD , Ait-Si-AliS , YokochiT , WadePA , JonesPL , WolffeAP. DNMT1 forms a complex with Rb, E2F1 and HDAC1 and represses transcription from E2F-responsive promoters. Nat. Genet.25(3), 338–342 (2000).
  • Razin A . CpG methylation, chromatin structure and gene silencing – a three-way connection. EMBO J.17(17), 4905–4908 (1998).
  • Henckel A , NakabayashiK , SanzLA , FeilR , HataK , ArnaudP. Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum. Mol. Genet.18(18), 3375–3383 (2009).
  • Luo C , HajkovaP , EckerJR. Dynamic DNA methylation: in the right place at the right time. Science361(6409), 1336–1340 (2018).
  • Moen EL , MarianiCJ , ZullowHet al. New themes in the biological functions of 5-methylcytosine and 5-hydroxymethylcytosine. Immunol. Rev.263(1), 36–49 (2015).
  • Yang X , HanH , DeCarvalho DD , LayFD , JonesPA , LiangG. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell26(4), 577–590 (2014).
  • Maunakea AK , NagarajanRP , BilenkyMet al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature466(7303), 253–257 (2010).
  • Smith ZD , MeissnerA. DNA methylation: roles in mammalian development. Nat. Rev. Genet.14(3), 204–220 (2013).
  • Meissner A , MikkelsenTS , GuHet al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature454(7205), 766–770 (2008).
  • Oakes CC , LaSalle S , SmiragliaDJ , RobaireB , TraslerJM. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev. Biol.307(2), 368–379 (2007).
  • Smallwood SA , KelseyG. De novo DNA methylation: a germ cell perspective. Trends Genet.28(1), 33–42 (2012).
  • Schisterman EF , SjaardaLA , ClemonsTet al. Effect of folic acid and zinc supplementation in men on semen quality and live birth among couples undergoing infertility treatment: a randomized clinical trial. JAMA323(1), 35–48 (2020).
  • Veron GL , TisseraAD , BelloRet al. Impact of age, clinical conditions, and lifestyle on routine semen parameters and sperm kinematics. Fertil. Steril.110(1), 68–75 e64 (2018).
  • Salas-Huetos A , BulloM , Salas-SalvadoJ. Dietary patterns, foods and nutrients in male fertility parameters and fecundability: a systematic review of observational studies. Hum. Reprod. Update23(4), 371–389 (2017).
  • Sharma R , HarlevA , AgarwalA , EstevesSC. Cigarette smoking and semen quality: a new meta-analysis examining the effect of the 2010 World Health Organization laboratory methods for the examination of human semen. Eur. Urol.70(4), 635–645 (2016).
  • Evans HJ , FletcherJ , TorranceM , HargreaveTB. Sperm abnormalities and cigarette smoking. Lancet1(8221), 627–629 (1981).
  • Senaldi L , Smith-RaskaM. Evidence for germline non-genetic inheritance of human phenotypes and diseases. Clinical Epigenetics12(1), 136 (2020).
  • Weigmann K . Lifestyle in the sperm: there is growing evidence that epigenetic marks can be inherited. But what is the nature of the information they store and over how many generations do they prevail?EMBO Reports15(12), 1233–1237 (2014).
  • Siddeek B , MauduitC , SimeoniU , BenahmedM. Sperm epigenome as a marker of environmental exposure and lifestyle, at the origin of diseases inheritance. Mutat. Res. Rev. Mutat. Res.778, 38–44 (2018).
  • Urdinguio RG , BayónGF , DmitrijevaMet al. Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum. Reprod.30(5), 1014–1028 (2015).
  • Aston KI , UrenPJ , JenkinsTGet al. Aberrant sperm DNA methylation predicts male fertility status and embryo quality. Fertil. Steril.104(6), 1388–1397.E5 (2015).
  • Jenkins TG , AstonKI , PfluegerC , CairnsBR , CarrellDT. Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLOS Genetics10(7), e1004458 (2014).
  • Jenkins TG , JamesER , AlonsoDFet al. Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology5(6), 1089–1099 (2017).
  • Jenkins TG , AstonKI , MeyerTDet al. Decreased fecundity and sperm DNA methylation patterns. Fertil. Steril.105(1), 51–57e51–e53 (2016).
  • Santana VP , JamesER , Miranda-FurtadoCLet al. Differential DNA methylation pattern and sperm quality in men with varicocele. Fertil. Steril.114(4), 770–778 (2020).
  • Marques PI , FernandesS , CarvalhoF , BarrosA , SousaM , MarquesCJ. DNA methylation imprinting errors in spermatogenic cells from maturation arrest azoospermic patients. Andrology5(3), 451–459 (2017).
  • Louie K , MinorA , NgR , PoonK , ChowV , MaS. Evaluation of DNA methylation at imprinted DMRs in the spermatozoa of oligozoospermic men in association with MTHFR C677T genotype. Andrology4(5), 825–831 (2016).
  • Wu X , LuoC , HuLet al. Unraveling epigenomic abnormality in azoospermic human males by WGBS, RNA-Seq, and transcriptome profiling analyses. J. Assist. Reprod. Genet.37(4), 789–802 (2020).
  • Laqqan M , TierlingS , AlkhaledY , LoPorto C , SolomayerEF , HammadehM. Spermatozoa from males with reduced fecundity exhibit differential DNA methylation patterns. Andrology5(5), 971–978 (2017).
  • Boissonnas CC , AbdalaouiHE , HaelewynVet al. Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men. Eur. J. Hum. Genet.18(1), 73–80 (2010).
  • He W , SunY , ZhangSet al. Profiling the DNA methylation patterns of imprinted genes in abnormal semen samples by next-generation bisulfite sequencing. J. Assist. Reprod. Genet.37(9), 2211–2221 (2020).
  • Sujit KM , SinghV , TrivediS , SinghK , GuptaG , RajenderS. Increased DNA methylation in the spermatogenesis-associated (SPATA) genes correlates with infertility. Andrology8(3), 602–609 (2020).
  • Navarro-Costa P , NogueiraP , CarvalhoMet al. Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum. Reprod.25(10), 2647–2654 (2010).
  • Barney R , StalkerK , LutesA , BaylesA , AstonK , JenkinsT. Assessment of seminal cell-free DNA as a potential contaminate in studies of human sperm DNA methylation. Andrology10(4), 702–709 (2022).
  • Krueger F . Trim Galore. https://github.com/FelixKrueger/TrimGalore
  • Krueger F , AndrewsSR. Bismark: a flexible aligner and methylation caller for bisulfite-seq applications. Bioinformatics (Oxford, England)27(11), 1571–1572 (2011).
  • Tarasov A , VilellaAJ , CuppenE , NijmanIJ , PrinsP. Sambamba: fast processing of NGS alignment formats. Bioinformatics (Oxford, England)31(12), 2032–2034 (2015).
  • Hansen KD , LangmeadB , IrizarryRA. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome biology13(10), R83 (2012).
  • Yu G , WangLG , HeQY. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics (Oxford, England)31(14), 2382–2383 (2015).
  • Korthauer K , ChakrabortyS , BenjaminiY , IrizarryRA. Detection and accurate false discovery rate control of differentially methylated regions from whole genome bisulfite sequencing. Biostatistics (Oxford, England)20(3), 367–383 (2019).
  • Gu Z . rGREAT: Client for GREAT Analysis (2021). https://github.com/jokergoo/rGREAT, http://great.stanford.edu/public/html/
  • Spiess AN , FeigC , SchulzeWet al. Cross-platform gene expression signature of human spermatogenic failure reveals inflammatory-like response. Hum. Reprod.22(11), 2936–2946 (2007).
  • Platts AE , DixDJ , ChemesHEet al. Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum. Mol. Genet.16(7), 763–773 (2007).
  • Mao S , WuF , CaoXet al. TDRP deficiency contributes to low sperm motility and is a potential risk factor for male infertility. Am. J. Transl. Res.8(1), 177–187 (2016).
  • Wang X , JiangH , ZhouWet al. Molecular cloning of a novel nuclear factor, TDRP1, in spermatogenic cells of testis and its relationship with spermatogenesis. Biochem. Biophys. Res. Commun.394(1), 29–35 (2010).
  • Lv M , LiuW , ChiWet al. Homozygous mutations in DZIP1 can induce asthenoteratospermia with severe MMAF. J. Med. Genet.57(7), 445–453 (2020).
  • Zariwala MA , KnowlesMR , LeighMW. Primary ciliary dyskinesia. In: GeneReviews.AdamMP, ArdingerHH, PagonRAet al.et al. ( Eds). University of Washington, WA, USA (1993).
  • Zhu X , DuY , LiDet al. Aberrant TGF-beta1 signaling activation by MAF underlies pathological lens growth in high myopia. Nat. Commun.12(1), 2102 (2021).
  • Hutchins JR , ToyodaY , HegemannBet al. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science328(5978), 593–599 (2010).
  • Hurt EM , WiestnerA , RosenwaldAet al. Overexpression of c-maf is a frequent oncogenic event in multiple myeloma that promotes proliferation and pathological interactions with bone marrow stroma. Cancer Cell5(2), 191–199 (2004).
  • Finkelstein M , EtkovitzN , BreitbartH. Ca(2+) signaling in mammalian spermatozoa. Mol. Cell. Endocrinol.516, 110953 (2020).
  • Martinez-Leon E , Osycka-SalutC , SignorelliJet al. Fibronectin stimulates human sperm capacitation through the cyclic AMP/protein kinase A pathway. Hum. Reprod.30(9), 2138–2151 (2015).
  • Jenkins TG , AstonKI , HotalingJM , ShamsiMB , SimonL , CarrellDT. Teratozoospermia and asthenozoospermia are associated with specific epigenetic signatures. Andrology4(5), 843–849 (2016).
  • Du Y , LiM , ChenJet al. Promoter targeted bisulfite sequencing reveals DNA methylation profiles associated with low sperm motility in asthenozoospermia. Hum. Reprod.31(1), 24–33 (2016).
  • Camprubí C , Salas-HuetosA , Aiese-CiglianoRet al. Spermatozoa from infertile patients exhibit differences of DNA methylation associated with spermatogenesis-related processes: an array-based analysis. Reprod. Biomed. Online33(6), 709–719 (2016).
  • Jones PA . Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nature Rev. Genetics13(7), 484–492 (2012).
  • Liu Y , DeboerK , DeKretser DMet al. LRGUK-1 is required for basal body and manchette function during spermatogenesis and male fertility. PLOS Genetics11(3), e1005090 (2015).
  • Papoutsopoulou S , NikolakakiE , ChalepakisG , KruftV , ChevaillierP , GiannakourosT. SR protein-specific kinase 1 is highly expressed in testis and phosphorylates protamine 1. Nucleic Acids Res.27(14), 2972–2980 (1999).