Research progress on the effect of sperm chromatin integrity on function and its detection methods
Received date: 2024-04-21
Revised date: 2024-06-29
Online published: 2024-07-05
Supported by
Baoding Science and Technology Plan Project(2341ZF280);Doctor Fund of Baoding No.1 Central Hospital
Sperm chromatin not only carries genetic information such as paternal DNA, but also carries structural proteins, epigenetic information, and higher-order chromatin structures (such as matrix attachment regions and telomeres), etc. These information play an important role in embryonic development. This article mainly reviews the effects of these different information carried by sperm chromatin on sperm function and embryonic development and the research progress of related detection methods, in order to provide a theoretical basis and scientific diagnosis and treatment strategies for the etiology screening of clinical infertility, embryo arrest and recurrent miscarriage, so as to improve the pregnancy outcomes of natural conception and assisted reproduction. Keywords: sperm chromatin; epigenetics; sperm DNA damage; sperm function; higher-order chromatin structures
Daiyuan Liu, Zhaohui Zhang, Xianjiang Kang . Research progress on the effect of sperm chromatin integrity on function and its detection methods[J]. Hereditas(Beijing), 2024 , 46(7) : 511 -529 . DOI: 10.16288/j.yczz.24-106
| [1] | Castillo J, Estanyol JM, Ballescá JL, Oliva R. Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility. Asian J Androl, 2015, 17(4): 601-609. |
| [2] | Farkouh A, Salvio G, Kuroda S, Saleh R, Vogiatzi P, Agarwal A. Sperm DNA integrity and male infertility: a narrative review and guide for the reproductive physicians. Transl Androl Urol, 2022, 11(7): 1023-1044. |
| [3] | Adler A, Roth B, Lundy SD, Takeshima T, Yumura Y, Kuroda S. Sperm DNA fragmentation testing in clinical management of reproductive medicine. Reprod Med Biol, 2023, 22(1): e12547. |
| [4] | Sureka R, Avvaru AK, Sowpati DT, Pathak RU, Mishra RK. Structural and developmental dynamics of Matrix associated regions in Drosophila melanogaster genome. BMC Genomics, 2022, 23(1): 725. |
| [5] | Du WL, Shi GJ, Shan CM, Li ZM, Zhu B, Jia ST, Li Q, Zhang ZG. Mechanisms of chromatin-based epigenetic inheritance. Sci China Life Sci, 2022, 65(11): 2162-2190. |
| [6] | Xu XM, Peng Q, Jiang XJ, Tan SM, Yang YQ, Yang WJ, Han YQ, Chen YY, Oyang LD, Lin JG, Xia LZ, Peng MJ, Wu NY, Tang YY, Li JY, Liao QJ, Zhou YJ. Metabolic reprogramming and epigenetic modifications in cancer: from the impacts and mechanisms to the treatment potential. Exp Mol Med, 2023, 55(7): 1357-1370. |
| [7] | Marcho C, Oluwayiose OA, Pilsner JR. The preconception environment and sperm epigenetics. Andrology, 2020, 8(4): 924-942. |
| [8] | Powell CD, Kirchoff DC, DeRouchey JE, Moseley HNB. Entropy based analysis of vertebrate sperm protamines sequences: evidence of potential dityrosine and cysteine- tyrosine cross-linking in sperm protamines. BMC Genomics, 2020, 21(1): 277. |
| [9] | Gòdia M, Lian Y, Naval-Sanchez M, Ponte I, Rodríguez-Gil JE, Sanchez A, Clop A. Micrococcal nuclease sequencing of porcine sperm suggests enriched co-location between retained histones and genomic regions related to semen quality and early embryo development. PeerJ, 2023, 11: e15520. |
| [10] | Ribas-Maynou J, Nguyen H, Valle R, Wu HW, Yeste M, Ward WS. Sperm degradation after vasectomy follows a sperm chromatin fragmentation-dependent mechanism causing DNA breaks in the toroid linker regions. Mol Hum Reprod, 2022, 29(9): gaac029. |
| [11] | Agarwal A, Majzoub A, Baskaran S, Panner Selvam MK, Cho CL, Henkel R, Finelli R, Leisegang K, Sengupta P, Barbarosie C, Parekh N, Alves MG, Ko E, Arafa M, Tadros N, Ramasamy R, Kavoussi P, Ambar R, Kuchakulla M, Robert KA, Iovine C, Durairajanayagam D, Jindal S, Shah R. Sperm DNA fragmentation: a new guideline for clinicians. World J Mens Health, 2020, 38(4): 412-471. |
| [12] | Barati E, Nikzad H, Karimian M. Oxidative stress and male infertility: current knowledge of pathophysiology and role of antioxidant therapy in disease management. Cell Mol Life Sci, 2020, 77(1): 93-113. |
| [13] | Tarozzi N, Bizzaro D, Flamigni C, Borini A. Clinical relevance of sperm DNA damage in assisted reproduction. Reprod Biomed Online, 2007, 14(6): 746-757. |
| [14] | Qiu Y, Yang H, Li CY, Xu CL. Progress in research on sperm DNA fragmentation. Med Sci Monit, 2020, 26: e918746. |
| [15] | Gualtieri R, Kalthur G, Barbato V, Longobardi S, Di Rella F, Adiga SK, Talevi R. Sperm oxidative stress during in vitro manipulation and its effects on sperm function and embryo development. Antioxidants (Basel), 2021, 10(7): 1025. |
| [16] | Andrabi SW, Ara A, Saharan A, Jaffar M, Gugnani N, Esteves SC. Sperm DNA fragmentation: causes, evaluation and management in male infertility. JBRA Assist Reprod, 2024, 28(2): 306-319. |
| [17] | Depuydt C, Donders G, Verstraete L, Beert J, Salembier G, Bosmans E, Dhont N, Kerkhofs C, Ombelet W. Negative impact of elevated DNA fragmentation and human papillomavirus (HPV) presence in sperm on the outcome of intra-uterine insemination (IUI). J Clin Med, 2021, 10(4): 717. |
| [18] | Arowolo O, Pilsner JR, Sergeyev O, Suvorov A. Mechanisms of male reproductive toxicity of polybrominated diphenyl ethers. Int J Mol Sci, 2022, 23(22): 14229. |
| [19] | Cui XR, Jing X, Wu XQ, Wang ZQ, Li Q. Potential effect of smoking on semen quality through DNA damage and the downregulation of Chk1 in sperm. Mol Med Rep, 2016, 14(1): 753-761. |
| [20] | Bareh GM, Jacoby E, Binkley P, Chang TCA, Schenken RS, Robinson RD. Sperm deoxyribonucleic acid fragmentation assessment in normozoospermic male partners of couples with unexplained recurrent pregnancy loss: a prospective study. Fertil Steril, 2016, 105(2): 329-336.e1. |
| [21] | Kumar K, Deka D, Singh A, Mitra DK, Vanitha BR, Dada R. Predictive value of DNA integrity analysis in idiopathic recurrent pregnancy loss following spontaneous conception. J Assist Reprod Genet, 2012, 29(9): 861-867. |
| [22] | Lu RJ, Chen X, Yu WJ, Jiang F, Zhou XY, Xu Y, Wang F. Analysis of age-associated alternation of SCSA sperm DNA fragmentation index and semen characteristics of 1790 subfertile males in China. J Clin Lab Anal, 2020, 34(12): e23548. |
| [23] | Hassanen E, Elqusi K, Zaki H, Henkel R, Agarwal A. TUNEL assay: establishing a sperm DNA fragmentation cut-off value for egyptian infertile men. Andrologia, 2019, 51(10): e13375. |
| [24] | Collins A, M?ller P, Gajski G, Vodenková S, Abdulwahed A, Anderson D, Bankoglu EE, Bonassi S, Boutet-Robinet E, Brunborg G, Chao C, Cooke MS, Costa C, Costa S, Dhawan A, de Lapuente J, Bo CD, Dubus J, Dusinska M, Duthie SJ, Yamani NE, Engelward B, Gaiv?o I, Giovannelli L, Godschalk R, Guilherme S, Gutzkow KB, Habas K, Hernández A, Herrero O, Isidori M, Jha AN, Knasmüller S, Kooter IM, Koppen G, Kruszewski M, Ladeira C, Laffon B, Larramendy M, Hégarat LL, Lewies A, Lewinska A, Liwszyc GE, de Cerain AL, Manjanatha M, Marcos R, Mili? M, de Andrade VM, Moretti M, Muruzabal D, Novak M, Oliveira R, Olsen AK, Owiti N, Pacheco M, Pandey AK, Pfuhler S, Pourrut B, Reisinger K, Rojas E, Rundén-Pran E, Sanz-Serrano J, Shaposhnikov S, Sipinen V, Smeets K, Stopper H, Teixeira JP, Valdiglesias V, Valverde M, van Acker F, van Schooten FJ, Vasquez M, Wentzel JF, Wnuk M, Wouters A, ?egura B, Zikmund T, Langie SAS, Azqueta A. Measuring DNA modifications with the comet assay: a compendium of protocols. Nat Protoc, 2023, 18(3): 929-989. |
| [25] | Chiorcea-Paquim AM. 8-oxoguanine and 8-oxodeoxyguanosine biomarkers of oxidative DNA damage: a review on HPLC-ECD determination. Molecules, 2022, 27(5): 1620. |
| [26] | Coban O, Serdarogullari M, Yarkiner Z, Serakinci N. Investigating the level of DNA double-strand break in human spermatozoa and its relation to semen characteristics and IVF outcome using phospho-histone H2AX antibody as a biomarker. Andrology, 2020, 8(2): 421-426. |
| [27] | Pourmasumi S, Khoradmehr A, Rahiminia T, Sabeti P, Talebi AR, Ghasemzadeh J. Evaluation of sperm chromatin integrity using aniline blue and toluidine blue staining in infertile and normozoospermic men. J Reprod Infertil, 2019, 20(2): 95-101. |
| [28] | Jahmani MY, Hammadeh ME, Al Smadi MA, Baller MK. Label-Free evaluation of chromatin condensation in human normal morphology sperm using Raman spectroscopy. Reprod Sci, 2021, 28(9): 2527-2539. |
| [29] | Majzoub A, Arafa M, El Ansari W, Mahdi M, Agarwal A, Al-Said S, Elbardisi H. Correlation of oxidation reduction potential and total motile sperm count: its utility in the evaluation of male fertility potential. Asian J Androl, 2020, 22(3): 317-322. |
| [30] | Rotondo JC, Lanzillotti C, Mazziotta C, Tognon M, Martini F. Epigenetics of male infertility: the role of DNA methylation. Front Cell Dev Biol, 2021, 9: 689624. |
| [31] | Kumaresan A, Das Gupta M, Datta TK, Morrell JM. Sperm DNA integrity and male fertility in farm animals: a review. Front Vet Sci, 2020, 7: 321. |
| [32] | Olszewska M, Barciszewska MZ, Fraczek M, Huleyuk N, Chernykh VB, Zastavna D, Barciszewski J, Kurpisz M. Global methylation status of sperm DNA in carriers of chromosome structural aberrations. Asian J Androl, 2017, 19(1): 117-124. |
| [33] | Ma RH, Zhang ZG, Zhang YT, Jian SY, Li BY. Detection of aberrant DNA methylation patterns in sperm of male recurrent spontaneous abortion patients. Zygote, 2023, 31(2): 163-172. |
| [34] | Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P, Bhattacharya S. A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update, 2014, 20(6): 840-852. |
| [35] | Carrell DT, Salas-Huetos A, Hotaling J. Increasing evidence of the role of the sperm epigenome in embryogenesis: oligoasthenoteratozoospermia, altered embryo DNA methylation, and miscarriage. Fertil Steril, 2018, 110(3): 401-402. |
| [36] | Hattori H, Hiura H, Kitamura A, Miyauchi N, Kobayashi N, Takahashi S, Okae H, Kyono K, Kagami M, Ogata T, Arima T. Association of four imprinting disorders and ART. Clin Epigenetics, 2019, 11(1): 21. |
| [37] | Oluwayiose OA, Wu HT, Saddiki H, Whitcomb BW, Balzer LB, Brandon N, Suvorov A, Tayyab R, Sites CK, Hill L, Marcho C, Pilsner JR. Sperm DNA methylation mediates the association of male age on reproductive outcomes among couples undergoing infertility treatment. Sci Rep, 2021, 11(1): 3216. |
| [38] | Alkhaled Y, Laqqan M, Tierling S, Lo Porto C, Amor H, Hammadeh ME. Impact of cigarette-smoking on sperm DNA methylation and its effect on sperm parameters. Andrologia, 2018. |
| [39] | Heikkinen A, Bollepalli S, Ollikainen M. The potential of DNA methylation as a biomarker for obesity and smoking. J Intern Med, 2022, 292(3): 390-408. |
| [40] | Rebuzzini P, Fabozzi G, Cimadomo D, Ubaldi FM, Rienzi L, Zuccotti M, Garagna S. Multi- and transgenerational effects of environmental toxicants on mammalian reproduction. Cells, 2022, 11(19): 3163. |
| [41] | Leanza C, Cannarella R, Barbagallo F, Gusmano C, Calogero AE. Does sperm SNRPN methylation change with fertility status and age? a systematic review and meta-regression analysis. Biomedicines, 2024, 12(2): 445. |
| [42] | Zhang WJ, Li M, Sun F, Xu XT, Zhang ZF, Liu JW, Sun XW, Zhang AP, Shen YP, Xu JH, Miao MH, Wu B, Yuan Y, Huang XL, Shi HJ, Du J. Association of sperm methylation at LINE-1, four candidate genes, and nicotine/alcohol exposure with the risk of infertility. Front Genet, 2019, 10: 1001. |
| [43] | Lee CW, Chen KL, Yuan CS, Lai CS, Tsai XY, Wu PH, Hsu PC. Epigenetic transgenerational effects of PM2.5 collected from southern Taiwan on sperm functions and DNA methylation in mouse offspring. Ecotoxicol Environ Saf, 2024, 269: 115802. |
| [44] | Tian YP, Zhou XY, Miao MH, Li DK, Wang ZL, Li RS, Liang H, Yuan W. Association of bisphenol A exposure with LINE-1 hydroxymethylation in human semen. Int J Environ Res Public Health, 2018, 15(8): 1770. |
| [45] | Presunto M, Mariana M, Lorigo M, Cairrao E. The effects of bisphenol A on human male infertility: a review of current epidemiological studies. Int J Mol Sci, 2023, 24(15): 12417. |
| [46] | Zheng HJ, Zhou XY, Li DK, Yang F, Pan HJ, Li TQ, Miao MH, Li RS, Yuan W. Genome-wide alteration in DNA hydroxymethylation in the sperm from bisphenol A-exposed men. PLoS One, 2017, 12(6): e0178535. |
| [47] | Ward WS. Function of sperm chromatin structural elements in fertilization and development. Mol Hum Reprod, 2010, 16(1): 30-36. |
| [48] | Bochyńska A, Lüscher-Firzlaff J, Lüscher B. Modes of interaction of KMT2 histone H3 lysine 4 methyltransferase/COMPASS complexes with chromatin. Cells, 2018, 7(3): 17. |
| [49] | Wang T, Gao H, Li W, Liu C. Essential role of histone replacement and modifications in male fertility. Front Genet, 2019, 10: 962. |
| [50] | Liu TT, Chen XX, Li TJ, Li XL, Lyu YH, Fan XT, Zhang PF, Zeng WX. Histone methyltransferase SETDB1 maintains survival of mouse spermatogonial stem/ progenitor cells via PTEN/AKT/FOXO1 pathway. Biochim Biophys Acta Gene Regul Mech, 2017, 1860(10): 1094-1102. |
| [51] | Dumasia K, Kumar A, Deshpande S, Balasinor NH. Estrogen, through estrogen receptor 1, regulates histone modifications and chromatin remodeling during spermatogenesis in adult rats. Epigenetics, 2017, 12(11): 953-963. |
| [52] | Okada Y, Scott G, Ray MK, Mishina Y, Zhang Y. Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature, 2007, 450(7166): 119-123. |
| [53] | Vallet-Buisan M, Mecca R, Jones C, Coward K, Yeste M. Contribution of semen to early embryo development: fertilization and beyond. Hum Reprod Update, 2023, 29(4): 395-433. |
| [54] | Soleymani Moud S, Kamal Seraji K, Ramezani M, Piravar Z. Association of single nucleotide polymorphisms in the PYGO2 and PRDM9 genes with idiopathic azoospermia in Iranian infertile male patients. Iran J Med Sci, 2023, 48(1): 77-84. |
| [55] | Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Sch?fer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell, 2001, 107(3): 323-337. |
| [56] | Zuo XL, Rong BW, Li L, Lv RT, Lan F, Tong MH. The histone methyltransferase SETD2 is required for expression of acrosin-binding protein 1 and protamines and essential for spermiogenesis in mice. J Biol Chem, 2018, 293(24): 9188-9197. |
| [57] | Blanco M, El Khattabi L, Gobé C, Crespo M, Coulée M, de la Iglesia A, Ialy-Radio C, Lapoujade C, Givelet M, Delessard M, Seller-Corona I, Yamaguchi K, Vernet N, Van Leeuwen F, Lermine A, Okada Y, Daveau R, Oliva R, Fouchet P, Ziyyat A, Pflieger D, Cocquet J. DOT1L regulates chromatin reorganization and gene expression during sperm differentiation. EMBO Rep, 2023, 24(6): e56316. |
| [58] | Pepin AS, Lafleur C, Lambrot R, Dumeaux V, Kimmins S. Sperm histone H3 lysine 4 tri-methylation serves as a metabolic sensor of paternal obesity and is associated with the inheritance of metabolic dysfunction. Mol Metab, 2022, 59: 101463. |
| [59] | Lismer A, Dumeaux V, Lafleur C, Lambrot R, Brind'Amour J, Lorincz MC, Kimmins S. Histone H3 lysine 4 trimethylation in sperm is transmitted to the embryo and associated with diet-induced phenotypes in the offspring. Dev Cell, 2021, 56(5): 671-686.e6. |
| [60] | Ma X, Fan Y, Xiao WW, Ding XW, Hu WY, Xia YK. Glufosinate-ammonium induced aberrant histone modifications in mouse sperm are concordant with transcriptome in preimplantation embryos. Front Physiol, 2021, 12: 819856. |
| [61] | Ashapkin V, Suvorov A, Pilsner JR, Krawetz SA, Sergeyev O. Age-associated epigenetic changes in mammalian sperm: implications for offspring health and development. Hum Reprod Update, 2023, 29(1): 24-44. |
| [62] | Pandya RK, Jijo A, Cheredath A, Uppangala S, Salian SR, Lakshmi VR, Kumar P, Kalthur G, Gupta S, Adiga SK. Differential sperm histone retention in normozoospermic ejaculates of infertile men negatively affects sperm functional competence and embryo quality. Andrology, 2024, 12(4): 881-890. |
| [63] | Fenic I, Hossain HM, Sonnack V, Tchatalbachev S, Thierer F, Trapp J, Failing K, Edler KS, Bergmann M, Jung M, Chakraborty T, Steger K. In vivo application of histone deacetylase inhibitor trichostatin-a impairs murine male meiosis. J Androl, 2008, 29(2): 172-185. |
| [64] | Doyon Y, Selleck W, Lane WS, Tan S, C?té J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol, 2004, 24(5): 1884-1896. |
| [65] | Dhillon VS, Shahid M, Deo P, Fenech M. Reduced SIRT1 and SIRT3 and lower antioxidant capacity of seminal plasma is associated with shorter sperm telomere length in oligospermic men. Int J Mol Sci, 2024, 25(2): 718. |
| [66] | Hada M, Masuda K, Yamaguchi K, Shirahige K, Okada Y. Identification of a variant-specific phosphorylation of TH2A during spermiogenesis. Sci Rep, 2017, 7: 46228. |
| [67] | Schon SB, Luense LJ, Wang XS, Bartolomei MS, Coutifaris C, Garcia BA, Berger SL. Histone modification signatures in human sperm distinguish clinical abnormalities. J Assist Reprod Genet, 2019, 36(2): 267-275. |
| [68] | Dhar S, Thota A, Rao MR. Insights into role of bromodomain, testis-specific (Brdt) in acetylated histone H4-dependent chromatin remodeling in mammalian spermiogenesis. J Biol Chem, 2012, 287(9): 6387-6405. |
| [69] | Shang EY, Nickerson HD, Wen DC, Wang XY, Wolgemuth DJ. The first bromodomain of Brdt, a testis-specific member of the BET sub-family of double- bromodomain- containing proteins, is essential for male germ cell differentiation. Development, 2007, 134(19): 3507-3515. |
| [70] | Ugur MR, Kutchy NA, de Menezes EB, Ul-Husna A, Haynes BP, Uzun A, Kaya A, Topper E, Moura A, Memili E. Retained acetylated histone four in bull sperm associated with fertility. Front Vet Sci, 2019, 6: 223. |
| [71] | Paradowska AS, Miller D, Spiess AN, Vieweg M, Cerna M, Dvorakova-Hortova K, Bartkuhn M, Schuppe HC, Weidner W, Steger K. Genome wide identification of promoter binding sites for H4K12ac in human sperm and its relevance for early embryonic development. Epigenetics, 2012, 7(9): 1057-1070. |
| [72] | Zhang ZH, Kang XJ, Mu SM. Histone phosphorylation and spermatogenesis. Hereditas (Beijing), 2014, 36(3): 220-227. |
| 张朝晖, 康现江, 穆淑梅. 组蛋白磷酸化修饰与精子发生. 遗传, 2014, 36(3): 220-227. | |
| [73] | Jha KN, Tripurani SK, Johnson GR. TSSK6 is required for γH2AX formation and the histone-to-protamine transition during spermiogenesis. J Cell Sci, 2017, 130(10): 1835-1844. |
| [74] | Pinto DMS, Flaus A. Structure and function of histone H2AX. Subcell Biochem, 2010, 50: 55-78. |
| [75] | Patankar A, Sudhakar DVS, Gajbhiye R, Surve S, Thangaraj K, Parte P. Proteomic and genetic dissection of testis-specific histone 2B in infertile men reveals its contribution to meiosis and sperm motility. F S Sci, 2022, 3(4): 322-330. |
| [76] | Zhang ZH, Mu SM, Guo MS, Wu JL, Li YQ, Zhang H, Wang Y, Kang XJ. Dynamics of histone H2A, H4 and HS1ph during spermatogenesis with a focus on chromatin condensation and maturity of spermatozoa. Sci Rep, 2016, 6: 25089. |
| [77] | Zhang ZH, Mu SM, Chen TR, Sun Z, Shu ZQ, Li YQ, Kang XJ. H4S1ph, an alternative epigenetic marker for sperm maturity. Andrologia, 2020, 52(1): e13352. |
| [78] | Sheng K, Liang XT, Huang SZ, Xu WM. The role of histone ubiquitination during spermatogenesis. Biomed Res Int, 2014, 2014: 870695. |
| [79] | Chen LJ, Xu WM, Yang M, Wang K, Chen Y, Huang XJ, Ma QH. HUWE1 plays important role in mouse preimplantation embryo development and the dysregulation is associated with poor embryo development in humans. Sci Rep, 2016, 6: 37928. |
| [80] | Sun JY, Zhu ZR, Li WW, Shen MY, Cao CH, Sun QC, Guo ZQ, Liu L, Wu DH. UBE2T-regulated H2AX monoubiquitination induces hepatocellular carcinoma radioresistance by facilitating CHK1 activation. J Exp Clin Cancer Res, 2020, 39(1): 222. |
| [81] | Gou LT, Kang JY, Dai P, Wang X, Li F, Zhao S, Zhang M, Hua MM, Lu Y, Zhu Y, Li Z, Chen H, Wu LG, Li DS, Fu XD, Li JS, Shi HJ, Liu MF. Ubiquitination-deficient mutations in human Piwi cause male infertility by impairing histone-to-protamine exchange during spermiogenesis. Cell, 2017, 169(6): 1090-1104.e13. |
| [82] | Meng CL, Liao JY, Zhao DF, Huang HH, Qin JZ, Lee TL, Chen DG, Chan WY, Xia Y. L3MBTL2 regulates chromatin remodeling during spermatogenesis. Cell Death Differ, 2019, 26(11): 2194-2207. |
| [83] | Wang XK, Kang JY, Wei LX, Yang XG, Sun HD, Yang SM, Lu L, Yan M, Bai MZ, Chen YY, Long JJ, Li N, Li DS, Huang J, Lei M, Shao Z, Yuan W, Zuo EW, Lu KH, Liu MF, Li JS. PHF7 is a novel histone H2A E3 ligase prior to histone-to-protamine exchange during spermiogenesis. Development, 2019, 146(13): dev175547. |
| [84] | Aoki VW, Emery BR, Liu LH, Carrell DT. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl, 2006, 27(6): 890-898. |
| [85] | Ge SQ, Zhao ZH, Zhang XQ, Hao Y. Epigenetic modifications in human spermatozoon and its potential role in embryonic development. Hereditas (Beijing), 2014, 36(5): 439-446. |
| 葛少钦, 赵峥辉, 张雪倩, 郝媛. 精子表观遗传修饰及其在胚胎发育过程中的潜在作用. 遗传, 2014, 36(5): 439-446. | |
| [86] | Balhorn R. The protamine family of sperm nuclear proteins. Genome Biol, 2007, 8(9): 227. |
| [87] | Castillo J, Amaral A, Oliva R. Sperm nuclear proteome and its epigenetic potential. Andrology, 2014, 2(3): 326-338. |
| [88] | de la Iglesia A, Jodar M, Oliva R, Castillo J. Insights into the sperm chromatin and implications for male infertility from a protein perspective. WIREs Mech Dis, 2023, 15(2): e1588. |
| [89] | Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB, Eddy EM. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet, 2001, 28(1): 82-86. |
| [90] | Cho C, Jung-Ha H, Willis WD, Goulding EH, Stein P, Xu Z, Schultz RM, Hecht NB, Eddy EM. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod, 2003, 69(1): 211-217. |
| [91] | Francis S, Yelumalai S, Jones C, Coward K. Aberrant protamine content in sperm and consequential implications for infertility treatment. Hum Fertil (Camb), 2014, 17(2): 80-89. |
| [92] | Jiang H, Huang CJ. Aberrant protamination in sperm correlates to anomalous nuclear and cytoplasmic architectures in infertile males with sperm dysmorphology. Asian J Androl, 2023, 26(2): 183-188. |
| [93] | Soler-Ventura A, Castillo J, de la Iglesia A, Jodar M, Barrachina F, Ballesca JL, Oliva R. Mammalian sperm protamine extraction and analysis: a step-by-step detailed protocol and brief review of protamine alterations. Protein Pept Lett, 2018, 25(5): 424-433. |
| [94] | Arévalo L, Merges GE, Schneider S, Oben FE, Neumann IS, Schorle H. Loss of the cleaved-protamine 2 domain leads to incomplete histone-to-protamine exchange and infertility in mice. PLoS Genet, 2022, 18(6): e1010272. |
| [95] | Rezaei-Gazik M, Vargas A, Amiri-Yekta A, Vitte AL, Akbari A, Barral S, Esmaeili V, Chuffart F, Sadighi- Gilani MA, Couté Y, Eftekhari-Yazdi P, Khochbin S, Rousseaux S, Totonchi M. Direct visualization of pre-protamine 2 detects protamine assembly failures and predicts ICSI success. Mol Hum Reprod, 2022, 28(2): gaac004. |
| [96] | Brunner AM, Nanni P, Mansuy IM. Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin, 2014, 7(1): 2. |
| [97] | Wu JY, Ribar TJ, Cummings DE, Burton KA, McKnight GS, Means AR. Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat Genet, 2000, 25(4): 448-452. |
| [98] | Schon SB, Moritz L, Rabbani M, Meguid J, Juliano BR, Ruotolo BT, Aston K, Hammoud SS. Proteomic analysis of human sperm reveals changes in protamine 1 phosphorylation in men with infertility. F S Sci, 2024, 5(2): 121-129. |
| [99] | Martisova A, Holcakova J, Izadi N, Sebuyoya R, Hrstka R, Bartosik M. DNA methylation in solid tumors: functions and methods of detection. Int J Mol Sci, 2021, 22(8): 4247. |
| [100] | Ben Maamar M, Sadler-Riggleman I, Beck D, Skinner MK. Genome-wide mapping of DNA methylation 5mC by methylated DNA immunoprecipitation (MeDIP)- sequencing. Methods Mol Biol, 2021, 2198: 301-310. |
| [101] | Cong WX, Li N, Wang JB, Kang Y, Miao YL, Xu CM, Wang ZQ, Liu TT, Gong L, Liu B, Ou XF. Genome-wide locus-specific DNA methylation repatterning may facilitate rapid evolution of mercury resistance in rice. Genes Genomics, 2022, 44(3): 299-306. |
| [102] | Honkova K, Rossnerova A, Chvojkova I, Milcova A, Margaryan H, Pastorkova A, Ambroz A, Rossner P Jr, Jirik V, Rubes J, Sram RJ, Topinka J. Genome-wide DNA methylation in policemen working in cities differing by major sources of air pollution. Int J Mol Sci, 2022, 23(3): 1666. |
| [103] | Ga?dzicka J, Biernacki K, Go??bek K, Mi?kiewicz- Orczyk K, Zi?ba N, Misio?ek M, Strzelczyk JK. Global DNA methylation level in tumour and margin samples in relation to human papilloma virus and epstein-barr virus in patients with oropharyngeal and oral squamous cell carcinomas. Biomedicines, 2024, 12(4): 914. |
| [104] | Uysal F, Kahveci S, Sukur G, Cinar O. Embryo culture media differentially alter DNA methylating enzymes and global DNA methylation in embryos and oocytes. J Mol Histol, 2022, 53(1): 63-74. |
| [105] | Heidari M, Darbandi M, Darbandi S, Sadeghi MR. Comparing the different methods of sperm chromatin assessment concerning ART outcomes. Turk J Urol, 2020, 46(5): 348-353. |
| [106] | Seligman J, Shalgi R, Oschry Y, Kosower NS. Sperm analysis by flow cytometry using the fluorescent thiol labeling agent monobromobimane. Mol Reprod Dev, 1991, 29(3): 276-281. |
| [107] | Schrott R, Modliszewski JL, Hawkey AB, Grenier C, Holloway Z, Evans J, Pippen E, Corcoran DL, Levin ED, Murphy SK. Sperm DNA methylation alterations from cannabis extract exposure are evident in offspring. Epigenetics Chromatin, 2022, 15(1): 33. |
| [108] | Khezri A, Narud B, Stenseth EB, Johannisson A, Myromslien FD, Gaustad AH, Wilson RC, Lyle R, Morrell JM, Kommisrud E, Ahmad R. DNA methylation patterns vary in boar sperm cells with different levels of DNA fragmentation. BMC Genomics, 2019, 20(1): 897. |
| [109] | Garrido N, Cruz F, Egea RR, Simon C, Sadler- Riggleman I, Beck D, Nilsson E, Ben Maamar M, Skinner MK. Sperm DNA methylation epimutation biomarker for paternal offspring autism susceptibility. Clin Epigenetics, 2021, 13(1): 6. |
| [110] | Montjean D, Zini A, Ravel C, Belloc S, Dalleac A, Copin H, Boyer P, McElreavey K, Benkhalifa M. Sperm global DNA methylation level: association with semen parameters and genome integrity. Andrology, 2015, 3(2): 235-240. |
| [111] | Peris-Frau P, álvarez-Rodríguez M, Martín-Maestro A, Iniesta-Cuerda M, Sánchez-Ajofrín I, Medina-Chávez DA, Garde JJ, Villar M, Rodríguez-Martínez H, Soler AJ. Unravelling how in vitro capacitation alters ram sperm chromatin before and after cryopreservation. Andrology, 2021, 9(1): 414-425. |
| [112] | Depincé A, Gabory A, Dziewulska K, Le Bail PY, Jammes H, Labbé C. DNA methylation stability in fish spermatozoa upon external constraint: impact of fish hormonal stimulation and sperm cryopreservation. Mol Reprod Dev, 2020, 87(1): 124-134. |
| [113] | de Mello F, Garcia JS, Godoy LC, Depincé A, Labbé C, Streit DP Jr. The effect of cryoprotectant agents on DNA methylation patterns and progeny development in the spermatozoa of Colossoma macropomum. Gen Comp Endocrinol, 2017, 245: 94-101. |
| [114] | Barzideh J, Scott RJ, Aitken RJ. Analysis of the global methylation status of human spermatozoa and its association with the tendency of these cells to enter apoptosis. Andrologia, 2013, 45(6): 424-429. |
| [115] | Cheung S, Parrella A, Tavares D, Keating D, Xie P, Rosenwaks Z, Palermo GD. Single-center thorough evaluation and targeted treatment of globozoospermic men. J Assist Reprod Genet, 2021, 38(8): 2073-2086. |
| [116] | Takeuchi Y, Sato S, Nagasato C, Motomura T, Okuda S, Kasahara M, Takahashi F, Yoshikawa S. Sperm-specific histone H1 in highly condensed sperm nucleus of Sargassum horneri. Sci Rep, 2024, 14(1): 3387. |
| [117] | Patankar A, Gajbhiye R, Surve S, Parte P. Epigenetic landscape of testis specific histone H2B variant and its influence on sperm function. Clin Epigenetics, 2021, 13(1): 101. |
| [118] | La Spina FA, Romanato M, Brugo-Olmedo S, De Vincentiis S, Julianelli V, Rivera RM, Buffone MG. Heterogeneous distribution of histone methylation in mature human sperm. J Assist Reprod Genet, 2014, 31(1): 45-49. |
| [119] | Kutchy NA, Velho A, Menezes ESB, Jacobsen M, Thibaudeau G, Wills RW, Moura A, Kaya A, Perkins A, Memili E. Testis specific histone 2B is associated with sperm chromatin dynamics and bull fertility-a pilot study. Reprod Biol Endocrinol, 2017, 15(1): 59. |
| [120] | Habibi M, Fakhari Zavareh Z, Abbasi B, Esmaeili V, Shahverdi A, Sadighi Gilani MA, Tavalaee M, Nasr-Esfahani MH. Alpha-lipoic acid supplementation for male partner of couples with recurrent pregnancy loss: a post hoc analysis in clinical trial. Int J Fertil Steril, 2023, 17(1): 67-74. |
| [121] | Lacalle E, Fernández-Alegre E, Gómez-Giménez B, álvarez-Rodríguez M, Martín-Fernández B, Soriano- úbeda C, Martínez-Pastor F. Application of flow cytometry using advanced chromatin analyses for assessing changes in sperm structure and DNA integrity in a porcine model. Int J Mol Sci, 2024, 25(4): 1953. |
| [122] | Ribas-Maynou J, Gawecka JE, Benet J, Ward WS. Double-stranded DNA breaks hidden in the neutral Comet assay suggest a role of the sperm nuclear matrix in DNA integrity maintenance. Mol Hum Reprod, 2014, 20(4): 330-340. |
| [123] | Gawecka JE, Ribas-Maynou J, Benet J, Ward WS. A model for the control of DNA integrity by the sperm nuclear matrix. Asian J Androl, 2015, 17(4): 610-615. |
| [124] | Johnson GD, Lalancette C, Linnemann AK, Leduc F, Boissonneault G, Krawetz SA. The sperm nucleus: chromatin, RNA, and the nuclear matrix. Reproduction, 2011, 141(1): 21-36. |
| [125] | Gawecka JE, Boaz S, Kasperson K, Nguyen H, Evenson DP, Ward WS. Luminal fluid of epididymis and vas deferens contributes to sperm chromatin fragmentation. Hum Reprod, 2015, 30(12): 2725-2736. |
| [126] | Shaman JA, Prisztoka R, Ward WS. Topoisomerase IIB and an extracellular nuclease interact to digest sperm DNA in an apoptotic-like manner. Biol Reprod, 2006, 75(5): 741-748. |
| [127] | Vi?olas-Vergés E, Yeste M, Garriga F, Bonet S, Mateo-Otero Y, Ribas-Maynou J. An intracellular, non-oxidative factor activates in vitro chromatin fragmentation in pig sperm. Biol Res, 2023, 56(1): 53. |
| [128] | Mir SM, Samavarchi Tehrani S, Goodarzi G, Jamalpoor Z, Asadi J, Khelghati N, Qujeq D, Maniati M. Shelterin complex at telomeres: implications in ageing. Clin Interv Aging, 2020, 15: 827-839. |
| [129] | Balmori C, Varela E. Should we consider telomere length and telomerase activity in male factor infertility? Curr Opin Obstet Gynecol, 2018, 30(3): 197-202. |
| [130] | Chieffi Baccari G, Iurato G, Santillo A, Dale B. Male germ cell telomeres and chemical pollutants. Biomolecules, 2023, 13(5): 745. |
| [131] | Lopes AC, Oliveira PF, Pinto S, Almeida C, Pinho MJ, Sá R, Rocha E, Barros A, Sousa M. Discordance between human sperm quality and telomere length following differential gradient separation/swim-up. J Assist Reprod Genet, 2020, 37(10): 2581-2603. |
| [132] | Ioannou D, Millan NM, Jordan E, Tempest HG. A new model of sperm nuclear architecture following assessment of the organization of centromeres and telomeres in three-dimensions. Sci Rep, 2017, 7: 41585. |
| [133] | Erdem HB, Bahsi T, Ergün MA. Function of telomere in aging and age related diseases. Environ Toxicol Pharmacol, 2021, 85: 103641. |
| [134] | Vyas CM, Ogata S, Reynolds CF, Mischoulon D, Chang G, Cook NR, Manson JE, Crous-Bou M, De Vivo I, Okereke OI. Telomere length and its relationships with lifestyle and behavioural factors: variations by sex and race/ethnicity. Age Ageing, 2021, 50(3): 838-846. |
| [135] | Gavia-García G, Rosado-Pérez J, Arista-Ugalde TL, Agui?iga-Sánchez I, Santiago-Osorio E, Mendoza- Nú?ez VM. Telomere length and oxidative stress and its relation with metabolic syndrome components in the aging. Biology (Basel), 2021, 10(4): 253. |
| [136] | Hemann MT, Rudolph KL, Strong MA, DePinho RA, Chin L, Greider CW. Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol Biol Cell, 2001, 12(7): 2023-2030. |
| [137] | Darmishonnejad Z, Zarei-Kheirabadi F, Tavalaee M, Zarei-Kheirabadi M, Zohrabi D, Nasr-Esfahani MH. Relationship between sperm telomere length and sperm quality in infertile men. Andrologia, 2020, 52(5): e13546. |
| [138] | Rocca MS, Speltra E, Menegazzo M, Garolla A, Foresta C, Ferlin A. Sperm telomere length as a parameter of sperm quality in normozoospermic men. Hum Reprod, 2016, 31(6): 1158-1163. |
| [139] | Moustakli E, Zikopoulos A, Sakaloglou P, Bouba I, Sofikitis N, Georgiou I. Functional association between telomeres, oxidation and mitochondria. Front Reprod Health, 2023, 5: 1107215. |
| [140] | Yang QL, Zhang N, Zhao FF, Zhao WL, Dai SJ, Liu JH, Bukhari I, Xin H, Niu WB, Sun YP. Processing of semen by density gradient centrifugation selects spermatozoa with longer telomeres for assisted reproduction techniques. Reprod Biomed Online, 2015, 31(1): 44-50. |
| [141] | Hanson BM, Tao X, Zhan YP, Kim JG, Klimczak AM, Herlihy NS, Scott RT Jr, Seli E. Shorter telomere length of white blood cells is associated with higher rates of aneuploidy among infertile women undergoing in vitro fertilization. Fertil Steril, 2021, 115(4): 957-965. |
| [142] | Telomeres Mendelian Randomization Collaboration, Haycock PC, Burgess S, Nounu A, Zheng J, Okoli GN, Bowden J, Wade KH, Timpson NJ, Evans DM, Willeit P, Aviv A, Gaunt TR, Hemani G, Mangino M, Ellis HP, Kurian KM, Pooley KA, Eeles RA, Lee JE, Fang SY, Chen WV, Law MH, Bowdler LM, Iles MM, Yang Q, Worrall BB, Markus HS, Hung RJ, Amos CI, Spurdle AB, Thompson DJ, O'Mara TA, Wolpin B, Amundadottir L, Stolzenberg-Solomon R, Trichopoulou A, Onland-Moret NC, Lund E, Duell EJ, Canzian F, Severi G, Overvad K, Gunter MJ, Tumino R, Svenson U, van Rij A, Baas AF, Bown MJ, Samani NJ, Tromp G, Jones GT, Kuivaniemi H, Elmore JR, Johansson M, McKay J, Scelo G, Carreras-Torres R, Gaborieau V, Brennan P, Bracci PM, Neale RE, Olson SH, Gallinger S, Li DH, Petersen GM, Risch HA, Klein AP, Han JL, Abnet CC, Freedman ND, Taylor PR, Maris JM, Aben KK, Kiemeney LA, Vermeulen SH, Wiencke JK, Walsh KM, Wrensch M, Rice T, Turnbull C, Litchfield K, Paternoster L, Standl M, Abecasis GR, SanGiovanni JP, Li Y, Mijatovic V, Sapkota Y, Low SK, Zondervan KT, Montgomery GW, Nyholt DR, van Heel DA, Hunt K, Arking DE, Ashar FN, Sotoodehnia N, Woo D, Rosand J, Comeau ME, Brown WM, Silverman EK, Hokanson JE, Cho MH, Hui JN, Ferreira MA, Thompson PJ, Morrison AC, Felix JF, Smith NL, Christiano AM, Petukhova L, Betz RC, Fan X, Zhang XJ, Zhu CH, Langefeld CD, Thompson SD, Wang FJ, Lin X, Schwartz DA, Fingerlin T, Rotter JI, Cotch MF, Jensen RA, Munz M, Dommisch H, Schaefer AS, Han F, Ollila HM, Hillary RP, Albagha O, Ralston SH, Zeng CJ, Zheng W, Shu XO, Reis A, Uebe S, Hüffmeier U, Kawamura Y, Otowa T, Sasaki T, Hibberd ML, Davila S, Xie G, Siminovitch K, Bei JX, Zeng YX, F?rsti A, Chen BW, Landi S, Franke A, Fischer A, Ellinghaus D, Flores C, Noth I, Ma SF, Foo JN, Liu JJ, Kim JW, Cox DG, Delattre O, Mirabeau O, Skibola CF, Tang CS, Garcia-Barcelo M, Chang KP, Su WH, Chang YS, Martin NG, Gordon S, Wade TD, Lee C, Kubo M, Cha PC, Nakamura Y, Levy D, Kimura M, Hwang SJ, Hunt S, Spector T, Soranzo N, Manichaikul AW, Barr RG, Kahali B, Speliotes E, Yerges-Armstrong LM, Cheng CY, Jonas JB, Wong TY, Fogh I, Lin K, Powell JF, Rice K, Relton CL, Martin RM, Davey Smith G. Association between telomere length and risk of cancer and non-neoplastic diseases: a mendelian randomization study. JAMA Oncol, 2017, 3(5): 636-651. |
| [143] | Lai TP, Wright WE, Shay JW. Comparison of telomere length measurement methods. Philos Trans R Soc Lond B Biol Sci, 2018, 373(1741): 20160451. |
| [144] | Demeke T, Dobnik D. Critical assessment of digital PCR for the detection and quantification of genetically modified organisms. Anal Bioanal Chem, 2018, 410(17): 4039-4050. |
| [145] | Luo YQ, Viswanathan R, Hande MP, Loh AHP, Cheow LF. Massively parallel single-molecule telomere length measurement with digital real-time PCR. Sci Adv, 2020, 6(34): eabb7944. |
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