{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T19:51:51Z","timestamp":1792439511470,"version":"4.5.0"},"reference-count":83,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2024,3,19]],"date-time":"2024-03-19T00:00:00Z","timestamp":1710806400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Infertility affects around 20% of couples of reproductive age; however, in some societies, as many as one-third of couples are unable to conceive. Different factors contribute to the decline of male fertility, such us environmental and professional exposure to endocrine disruptors, oxidative stress, and life habits with the risk of de novo epigenetics dysregulation. Since the fantastic development of new \u201comes and omics\u201d technologies, the contribution of inherited or de novo genomes and epigenome disorders to male infertility have been further elucidated. Many other techniques have become available to andrology laboratories for the investigation of genome and epigenome integrity and the maturation and the competency of spermatozoa. All these new methods of assessment are highlighting the importance of genetics and epigenetics investigation for assisted reproduction pathology and for supporting professionals in counselling patients and proposing different management strategies for male infertility. This aims to improve clinical outcomes while minimizing the risk of genetics or health problems at birth.<\/jats:p>","DOI":"10.3390\/genes15030377","type":"journal-article","created":{"date-parts":[[2024,3,19]],"date-time":"2024-03-19T09:39:31Z","timestamp":1710841171000},"page":"377","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["Genome and Epigenome Disorders and Male Infertility: Feedback from 15 Years of Clinical and Research Experience"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9776-7459","authenticated-orcid":false,"given":"Debbie","family":"Montjean","sequence":"first","affiliation":[{"name":"Fertilys Fertility Centers Laval and Brossard, 1950 Maurice-Gauvin Street, Laval, QC H7S 1Z5, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marion","family":"Beaumont","sequence":"additional","affiliation":[{"name":"Genetics Department, Eylau\/Unilabs Laboratory, 92110 Clichy, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abdelhafid","family":"Natiq","sequence":"additional","affiliation":[{"name":"Center for Genomics of Human Pathologies (GENOPATH), Faculty of Medicine and Pharmacy, University Mohammed V of Rabat, Rabat, Morocco"},{"name":"National Laboratory Mohammed VI, Mohammed VI Foundation of Casablanca, Casablanca, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Noureddine","family":"Louanjli","sequence":"additional","affiliation":[{"name":"Andro-Genetics Unit, Labomac, Casablanca, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andre","family":"Hazout","sequence":"additional","affiliation":[{"name":"Andro-Genetics Unit, Labomac, Casablanca, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3509-2369","authenticated-orcid":false,"given":"Pierre","family":"Miron","sequence":"additional","affiliation":[{"name":"Fertilys Fertility Centers Laval and Brossard, 1950 Maurice-Gauvin Street, Laval, QC H7S 1Z5, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Liehr","sequence":"additional","affiliation":[{"name":"Institute f\u00fcr Humangenetik, Universit\u00e4tsklinikum Jena, Friedrich Schiller Universit\u00e4t, 07743 Jena, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosalie","family":"Cabry","sequence":"additional","affiliation":[{"name":"Reproductive Medicine, Reproductive Biology & Genetics, CECOS Picardie, University Hospital & School of Medicine, Picardie University Jules Verne, 80000 Amiens, France"},{"name":"PeriTox Laboratory, Perinatality & Toxic Risks, UMR-I 01 INERIS, Picardie University Jules Verne, 80000 Amiens, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7569-739X","authenticated-orcid":false,"given":"Ilham","family":"Ratbi","sequence":"additional","affiliation":[{"name":"Center for Genomics of Human Pathologies (GENOPATH), Faculty of Medicine and Pharmacy, University Mohammed V of Rabat, Rabat, Morocco"},{"name":"Medical Genetics Unit, Ibn Sina University Hospital Center, Rabat, Morocco"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Moncef","family":"Benkhalifa","sequence":"additional","affiliation":[{"name":"Fertilys Fertility Centers Laval and Brossard, 1950 Maurice-Gauvin Street, Laval, QC H7S 1Z5, Canada"},{"name":"Reproductive Medicine, Reproductive Biology & Genetics, CECOS Picardie, University Hospital & School of Medicine, Picardie University Jules Verne, 80000 Amiens, France"},{"name":"PeriTox Laboratory, Perinatality & Toxic Risks, UMR-I 01 INERIS, Picardie University Jules Verne, 80000 Amiens, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Boitrelle, F., Shah, R., Saleh, R., Henkel, R., Kandil, H., Chung, E., Vogiatzi, P., Zini, A., Arafa, M., and Agarwal, A. (2021). The Sixth Edition of the WHO Manual for Human Semen Analysis: A Critical Review and SWOT Analysis. Life, 11.","DOI":"10.3390\/life11121368"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/bmb\/ldab025","article-title":"Translational aspects of novel findings in genetics of male infertility-status quo 2021","volume":"140","author":"Laan","year":"2021","journal-title":"Br. Med. Bull."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/BF00278879","article-title":"Localization of factors controlling spermatogenesis in the nonfluorescent portion of the human Y chromosome long arm","volume":"34","author":"Tiepolo","year":"1976","journal-title":"Hum. Genet."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1056\/NEJMoa0806218","article-title":"Spermatogenesis in a man with complete deletion of USP9Y","volume":"360","author":"Luddi","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2333","DOI":"10.1093\/hmg\/ddh240","article-title":"The AZFa gene DBY (DDX3Y) is widely transcribed but the protein is limited to the male germ cells by translation control","volume":"13","author":"Ditton","year":"2004","journal-title":"Hum. Mol. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"659","DOI":"10.5534\/wjmh.220089","article-title":"Bridging the Gap between AZF Microdeletions and Karyotype: Twelve Years\u2019 Experience of an Infertility Center","volume":"41","author":"Kalantari","year":"2023","journal-title":"World J. Men\u2019s Health"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/aja.2010.101","article-title":"Mouse models in male fertility research","volume":"13","author":"Jamsai","year":"2011","journal-title":"Asian J. Androl."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/humupd\/dmab030","article-title":"A systematic review of the validated monogenic causes of human male infertility: 2020 update and a discussion of emerging gene-disease relationships","volume":"28","author":"Houston","year":"2021","journal-title":"Hum. Reprod. Update"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"217","DOI":"10.4103\/jhrs.jhrs_115_21","article-title":"Genetics of Male Infertility\u2014Present and Future: A Narrative Review","volume":"14","author":"Sudhakar","year":"2021","journal-title":"J. Hum. Reprod. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.aju.2017.11.002","article-title":"Role of sperm DNA fragmentation in male factor infertility: A systematic review","volume":"16","author":"Cho","year":"2018","journal-title":"Arab. J. Urol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"104","DOI":"10.5534\/wjmh.200195","article-title":"Advanced Paternal Age and Sperm DNA Fragmentation: A Systematic Review","volume":"40","author":"Gonzalez","year":"2022","journal-title":"World J. Men\u2019s Health"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.maturitas.2014.02.011","article-title":"How to overcome male infertility after 40: Influence of paternal age on fertility","volume":"78","author":"Belloc","year":"2014","journal-title":"Maturitas"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1586\/14737159.2014.864558","article-title":"Emerging molecular methods for male infertility investigation","volume":"14","author":"Benkhalifa","year":"2014","journal-title":"Expert Rev. Mol. Diagn."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1016\/S0140-6736(95)91768-3","article-title":"Sex chromosome abnormalities after intracytoplasmic sperm injection","volume":"346","author":"Liebaers","year":"1995","journal-title":"Lancet"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1095\/biolreprod.107.065623","article-title":"Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring","volume":"78","author":"Moreira","year":"2008","journal-title":"Biol. Reprod."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3109\/19396368.2010.515704","article-title":"Are sperm chromatin and DNA defects relevant in the clinic?","volume":"57","author":"Zini","year":"2011","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2908","DOI":"10.1093\/humrep\/des261","article-title":"The effect of sperm DNA fragmentation on miscarriage rates: A systematic review and meta-analysis","volume":"27","author":"Robinson","year":"2012","journal-title":"Hum. Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1016\/S0015-0282(03)01151-8","article-title":"Quantitation by image analysis of global DNA methylation in human spermatozoa and its prognostic value in in vitro fertilization: A preliminary study","volume":"80","author":"Benchaib","year":"2003","journal-title":"Fertil. Steril."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.fertnstert.2006.05.057","article-title":"Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome","volume":"87","author":"Benchaib","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1508","DOI":"10.1016\/j.fertnstert.2014.10.008","article-title":"Perspectives on the assessment of human sperm chromatin integrity","volume":"102","author":"Palermo","year":"2014","journal-title":"Fertil. Steril."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1283","DOI":"10.1177\/0300060516664240","article-title":"Effect of sperm DNA fragmentation on clinical outcomes for Chinese couples undergoing in vitro fertilization or intracytoplasmic sperm injection","volume":"44","author":"Xue","year":"2016","journal-title":"J. Int. Med. Res."},{"key":"ref_22","first-page":"343","article-title":"Effect of sperm DNA fragmentation on embryo development: Clinical and biological aspects","volume":"21","author":"Bilinski","year":"2017","journal-title":"JBRA Assist. Reprod."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.bpobgyn.2017.07.003","article-title":"Review: Diagnosis and impact of sperm DNA alterations in assisted reproduction","volume":"44","author":"Simon","year":"2017","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1953","DOI":"10.1007\/s10815-018-1304-4","article-title":"Paternal factors contributing to embryo quality","volume":"35","author":"Colaco","year":"2018","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1093\/humupd\/dml057","article-title":"Altered protamine expression and diminished spermatogenesis: What is the link?","volume":"13","author":"Carrell","year":"2007","journal-title":"Hum. Reprod. Update"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1093\/molehr\/gap056","article-title":"Mutations in the protamine locus: Association with spermatogenic failure?","volume":"15","author":"Imken","year":"2009","journal-title":"Mol. Hum. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1056\/NEJMoa0806228","article-title":"Mutations in NR5A1 associated with ovarian insufficiency","volume":"360","author":"Brauner","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1016\/j.ajhg.2010.09.009","article-title":"Human Male Infertility Associated with Mutations in NR5A1 Encoding Steroidogenic Factor 1","volume":"87","author":"Bashamboo","year":"2010","journal-title":"Am. J. Hum. Genet."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2013","DOI":"10.1111\/j.1572-0241.1998.02013.x","article-title":"Folate and colorectal carcinogenesis: Is DNA repair the missing link?","volume":"93","author":"Choi","year":"1998","journal-title":"Am. J. Gastroenterol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1016\/S0015-0282(03)02157-5","article-title":"C677T methylenetetrahydrofolate reductase polymorphism interferes with the effects of folic acid and zinc sulfate on sperm concentration","volume":"80","author":"Ebisch","year":"2003","journal-title":"Fertil. Steril."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1016\/j.fertnstert.2010.08.054","article-title":"Polymorphisms in MTHFR and MTRR genes associated with blood plasma homocysteine concentration and sperm counts","volume":"95","author":"Montjean","year":"2011","journal-title":"Fertil. Steril."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1093\/molehr\/gam009","article-title":"Expression of CatSper family transcripts in the mouse testis during post-natal development and human ejaculated spermatozoa: Relationship to sperm motility","volume":"13","author":"Li","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1957","DOI":"10.1093\/humrep\/den193","article-title":"Mutations in dynein genes in patients affected by isolated non-syndromic asthenozoospermia","volume":"23","author":"Zuccarello","year":"2008","journal-title":"Hum. Reprod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1038\/ng2027","article-title":"Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility","volume":"39","author":"Dieterich","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1086\/521314","article-title":"Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia","volume":"81","author":"Dam","year":"2007","journal-title":"Am. J. Hum. Genet."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/j.ajhg.2011.02.007","article-title":"A Recurrent Deletion of DPY19L2 Causes Infertility in Man by Blocking Sperm Head Elongation and Acrosome Formation","volume":"88","author":"Harbuz","year":"2011","journal-title":"Am. J. Hum. Genet."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1093\/humrep\/den280","article-title":"The pattern of localization of the putative oocyte activation factor, phospholipase Czeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa","volume":"23","author":"Grasa","year":"2008","journal-title":"Hum. Reprod."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3609","DOI":"10.1016\/j.febslet.2013.10.008","article-title":"Sperm PLC\u03b6: From structure to Ca2+ oscillations, egg activation and therapeutic potential","volume":"587","author":"Nomikos","year":"2013","journal-title":"FEBS Lett."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Saleh, A., Kashir, J., Thanassoulas, A., Safieh-Garabedian, B., Lai, F.A., and Nomikos, M. (2020). Essential Role of Sperm-Specific PLC-Zeta in Egg Activation and Male Factor Infertility: An Update. Front. Cell Dev. Biol., 8.","DOI":"10.3389\/fcell.2020.00028"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1038\/s41598-018-19497-6","article-title":"Sperm-borne phospholipase C zeta-1 ensures monospermic fertilization in mice","volume":"8","author":"Nozawa","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3533","DOI":"10.1242\/dev.129.15.3533","article-title":"PLC zeta: A sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development","volume":"129","author":"Saunders","year":"2002","journal-title":"Development"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"10408","DOI":"10.1074\/jbc.M313801200","article-title":"Recombinant phospholipase Czeta has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs","volume":"279","author":"Kouchi","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3671","DOI":"10.1172\/JCI36942","article-title":"Human sperm devoid of PLC, zeta 1 fail to induce Ca(2+) release and are unable to initiate the first step of embryo development","volume":"118","author":"Yoon","year":"2008","journal-title":"J. Clin. Invest."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.rbmo.2014.11.012","article-title":"Live birth after artificial oocyte activation using a ready-to-use ionophore: A prospective multicentre study","volume":"30","author":"Ebner","year":"2015","journal-title":"Reprod. Biomed. Online"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.fertnstert.2019.04.006","article-title":"Assisted oocyte activation significantly increases fertilization and pregnancy outcome in patients with low and total failed fertilization after intracytoplasmic sperm injection: A 17-year retrospective study","volume":"112","author":"Bonte","year":"2019","journal-title":"Fertil. Steril."},{"key":"ref_46","first-page":"3","article-title":"Effect of Artificial Oocyte Activation on Intra-Cytoplasmic Sperm Injection Outcomes in Patients with Lower Percentage of Sperm Containing Phospholipase C\u03b6: A Randomized Clinical Trial","volume":"20","author":"Nazarian","year":"2019","journal-title":"J. Reprod. Infertil."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.tibs.2005.12.008","article-title":"Genomic DNA methylation: The mark and its mediators","volume":"31","author":"Klose","year":"2006","journal-title":"Trends Biochem. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.ceb.2007.04.002","article-title":"Mechanisms of epigenetic inheritance","volume":"19","author":"Martin","year":"2007","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1530\/REP-09-0281","article-title":"Paternal DNA packaging in spermatozoa: More than the sum of its parts? DNA, histones, protamines and epigenetics","volume":"139","author":"Miller","year":"2010","journal-title":"Reproduction"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1071\/RD10197","article-title":"Presence of histone H3 acetylated at lysine 9 in male germ cells and its distribution pattern in the genome of human spermatozoa","volume":"23","author":"Steilmann","year":"2011","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1046\/j.1439-0272.2002.00524.x","article-title":"Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis","volume":"34","author":"Sonnack","year":"2002","journal-title":"Andrologia"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1007\/s10815-018-1354-7","article-title":"Histone modification signatures in human sperm distinguish clinical abnormalities","volume":"36","author":"Schon","year":"2019","journal-title":"Assist. Reprod. Genet."},{"key":"ref_53","first-page":"3","article-title":"H3K4me2 accompanies chromatin immaturity in human spermatozoa: An epigenetic marker for sperm quality assessment","volume":"66","author":"Sutovsky","year":"2019","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"aab2006","DOI":"10.1126\/science.aab2006","article-title":"Disruption of histone methylation in developing sperm impairs offspring health transgenerationally","volume":"350","author":"Siklenka","year":"2015","journal-title":"Science"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"895502","DOI":"10.3389\/fendo.2022.895502","article-title":"The Art of Packaging the Sperm Genome: Molecular and Structural Basis of the Histone-To-Protamine Exchange","volume":"13","author":"Moritz","year":"2022","journal-title":"Front. Endocrinol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Ravel, C., Chantot-Bastaraud, S., El Houate, B., Berthaut, I., Verstraete, L., De Larouziere, V., Louren\u00e7o, D., Dumaine, A., Antoine, J.M., and Mandelbaum, J. (2007). Mutations in the protamine 1 gene associated with male infertility. Mol. Hum. Reprod., 461\u2013464.","DOI":"10.1093\/molehr\/gam031"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1099270","DOI":"10.3389\/fendo.2022.1099270","article-title":"Deleterious variants in TAF7L cause human oligoasthenoteratozoospermia and its impairing histone to protamine exchange inducing reduced in vitro fertilization","volume":"13","author":"Bai","year":"2023","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1002\/j.1939-4640.2005.tb02874.x","article-title":"A suite of novel human spermatozoal RNAs","volume":"26","author":"Ostermeier","year":"2005","journal-title":"J. Androl."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1186\/1479-7364-3-2-195","article-title":"Analysis and update of the human solute carrier (SLC) gene superfamily","volume":"3","author":"He","year":"2009","journal-title":"Hum. Genom."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"435","DOI":"10.3389\/fendo.2019.00435","article-title":"Expression Patterns of Circular RNAs in High Quality and Poor Quality Human Spermatozoa","volume":"10","author":"Chioccarelli","year":"2019","journal-title":"Front. Endocrinol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1293368","DOI":"10.3389\/fendo.2024.1293368","article-title":"MicroRNAs in spermatogenesis dysfunction and male infertility: Clinical phenotypes, mechanisms and potential diagnostic biomarkers","volume":"15","author":"Shi","year":"2024","journal-title":"Front. Endocrinol. (Lausanne)"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1095\/biolreprod55.5.1155","article-title":"Developmental exposure of male germ cells to 5-azacytidine results in abnormal preimplantation development in rats","volume":"55","author":"Doerksen","year":"1996","journal-title":"Biol. Reprod."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/nature02625","article-title":"Epigenetics in human disease and prospects for epigenetic therapy","volume":"429","author":"Egger","year":"2004","journal-title":"Nature"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1700","DOI":"10.1016\/S0140-6736(04)16256-9","article-title":"Genomic imprinting in disruptive spermatogenesis","volume":"363","author":"Marques","year":"2004","journal-title":"Lancet"},{"key":"ref_65","doi-asserted-by":"crossref","unstructured":"Houshdaran, S., Cortessis, V.K., Siegmund, K., Yang, A., Laird, P.W., and Sokol, R.Z. (2007). Widespread epigenetic abnormalities suggest a broad DNA methylation erasure defect in abnormal human sperm. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0001289"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"2542","DOI":"10.1093\/hmg\/ddm187","article-title":"Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients","volume":"16","author":"Kobayashi","year":"2007","journal-title":"Hum. Mol. Genet."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1093\/molehr\/gam093","article-title":"Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia","volume":"14","author":"Marques","year":"2008","journal-title":"Mol. Hum. Reprod."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1038\/ejhg.2009.117","article-title":"Specific epigenetic alterations of IGF2-H19 locus in spermatozoa from infertile men","volume":"18","author":"Boissonnas","year":"2010","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.1016\/j.fertnstert.2013.06.047","article-title":"Methylation changes in mature sperm deoxyribonucleic acid from oligozoospermic men: Assessment of genetic variants and assisted reproductive technology outcome","volume":"100","author":"Montjean","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.4161\/15592294.2014.988063","article-title":"Epigenetic heterogeneity of developmentally important genes in human sperm: Implications for assisted reproduction outcome","volume":"9","author":"Kuhtz","year":"2015","journal-title":"Epigenetics"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1295","DOI":"10.1093\/hmg\/ddu540","article-title":"Epigenetic germline mosaicism in infertile men","volume":"24","author":"Laurentino","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1111\/andr.12001","article-title":"Sperm global DNA methylation level: Association with semen parameters and genome integrity","volume":"3","author":"Montjean","year":"2015","journal-title":"Andrology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1093\/humrep\/dev053","article-title":"Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility","volume":"30","author":"Urdinguio","year":"2015","journal-title":"Hum. Reprod."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1466","DOI":"10.1126\/science.1108190","article-title":"Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility","volume":"308","author":"Anway","year":"2005","journal-title":"Science"},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Manikkam, M., Tracey, R., Guerrero-Bosagna, C., and Skinner, M.K. (2013). Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0055387"},{"key":"ref_76","unstructured":"Liehr, T. (2021). Cytogenomics [Internet], Academic Press. Available online: https:\/\/www.sciencedirect.com\/science\/article\/pii\/B9780128235799000114."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1186\/1755-8166-1-25","article-title":"Chromosome distribution in human sperm\u2014A 3D multicolor banding-study","volume":"1","author":"Manvelyan","year":"2008","journal-title":"Mol. Cytogenet."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"32","DOI":"10.3109\/19396368.2014.979956","article-title":"Small supernumerary marker chromosomes and the nuclear architecture of sperm\u2014A study in a fertile and an infertile brother","volume":"61","author":"Karamysheva","year":"2015","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1159\/000491870","article-title":"Impaired Spermatogenesis due to Small Supernumerary Marker Chromosomes: The Reason for Infertility Is Only Reliably Ascertainable by Cytogenetics","volume":"12","author":"Liehr","year":"2018","journal-title":"Sex. Dev."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1038\/aja.2009.65","article-title":"Quick recovery and characterization of cell-free DNA in seminal plasma of normozoospermia and azoospermia: Implications for non-invasive genetic utilities","volume":"11","author":"Li","year":"2009","journal-title":"Asian J. Androl."},{"key":"ref_81","first-page":"e13822","article-title":"Seminal cell-free DNA and sperm characteristic\u2019s: An added biomarker for male infertility investigation","volume":"53","author":"Celton","year":"2021","journal-title":"Andrologia"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1016\/j.fertnstert.2013.01.125","article-title":"Are imprinting disorders more prevalent after human in vitro fertilization or intracytoplasmic sperm injection?","volume":"99","author":"Vermeiden","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Li, Y., Li, Q., Wu, L., Wang, H., Shi, H., Yang, C., Gu, Y., Li, J., and Ji, Z. (2024). SperMD: The expression atlas of sperm maturation. BMC Bioinform., 25.","DOI":"10.1186\/s12859-024-05631-x"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/15\/3\/377\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:15:55Z","timestamp":1760105755000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/15\/3\/377"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,19]]},"references-count":83,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["genes15030377"],"URL":"https:\/\/doi.org\/10.3390\/genes15030377","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,19]]}}}