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Chapter 10 - Aging and Environmental Interactions with the Sperm Epigenome

from Section 2 - The Biology of Male Reproduction and Infertility

Published online by Cambridge University Press:  06 December 2023

By
Albert Salas-Huetos  and
Douglas T. Carrell
Edited by
Douglas T. Carrell ,
Alexander W. Pastuszak  and
James M. Hotaling
Douglas T. Carrell
Affiliation:
Utah Center for Reproductive Medicine
Alexander W. Pastuszak
Affiliation:
University of Utah
James M. Hotaling
Affiliation:
Utah Center for Reproductive Medicine
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Summary

The definition of epigenetics has been redefined in the last decades and today is generally accepted as the study of heritable factors, other than DNA base pair coding, that regulate gene expression. In this chapter, we briefly review the main epigenetic factors that exist in spermatozoa (e.g., histone and chromatin modifications, DNA methylation, and noncoding RNAs [ncRNAs]) and underline the associations and effects of aging, adiposity, and some lifestyle and environmental factors on the sperm epigenome. In conclusion, further work needs to be done to establish whether the changes of sperm epigenome triggered by aging, adiposity, diet, and smoking can have not only implications for the reproductive health but also for the future offspring.

Keywords

spermepigeneticsagingobesitylifestyle factorsenvironmental factors
Type
Chapter
Information
Men's Reproductive and Sexual Health Throughout the Lifespan
An Integrated Approach to Fertility, Sexual Function, and Vitality
 , pp. 81 - 86
Publisher: Cambridge University Press
Print publication year: 2023

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References

Waddington, CH. The epigenotype. 1942. Int J Epidemiol. 2012;41(1):10–13.CrossRefGoogle ScholarPubMed
Waddington, CH. Towards a theoretical biology. Nature. 1968;218:525–527.Google Scholar
Santana, V, Salas-Huetos, A, James, ER, Carrell, DT. The effect of endocrine disruptors and environmental and lifestyle factors on the sperm epigenome. In: Aitken, RJ, Mortimer, D, Kovacs, G, eds. Male and Sperm Factors That Maximize IVF Success. Cambridge University Press; 2020:41–58.CrossRefGoogle Scholar
Jones, RE, Lopez, KH. Human Reproductive Biology. 4th ed. Academic Press; 2004.Google Scholar
Schagdarsurengin, U, Paradowska, A, Steger, K. Analysing the sperm epigenome: roles in early embryogenesis and assisted reproduction. Nat Rev Urol. 2012;9(11):609–619.CrossRefGoogle ScholarPubMed
Bowman, GD, Poirier, MG. Post-translational modifications of histones that influence nucleosome dynamics. Chem Rev. 2015;115(6):2274–2295.CrossRefGoogle ScholarPubMed
Oliva, R. Protamines and male infertility. Hum Reprod Update. 2006;12(4):417–435.Google Scholar
Oliva, R, Castillo, J, Estanyol, J, Ballescà, J. Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility. Asian J Androl. 2015;17(4):601–609.CrossRefGoogle Scholar
Hammoud, SS, Nix, DA, Zhang, H, Purwar, J, Carrell, DT, Cairns, BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009;460(7254):473–478.Google Scholar
Brykczynska, U, Hisano, M, Erkek, S, et al. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol. 2010;17(6):679–687.CrossRefGoogle ScholarPubMed
Jin, B, Li, Y, Robertson, KD. DNA methylation: superior or subordinate in the epigenetic hierarchy? Genes Cancer. 2011;2(6):607–617.CrossRefGoogle ScholarPubMed
Camprubí, C, Cigliano, RA, Salas-Huetos, A, Garrido, N, Blanco, J. What the human sperm methylome tells us. Epigenomics. 2017;9(10):1299–1315.Google Scholar
Ha, M, Kim, VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol [Internet]. 2014 [cited 2014 Jul 17];15(8):509–524. Available from: www.ncbi.nlm.nih.gov/pubmed/25027649Google Scholar
O’Brien, J, Hayder, H, Zayed, Y, Peng, C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:1–12.Google ScholarPubMed
Kozomara, A, Griffiths-Jones, S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 2011;39:D152–D157.CrossRefGoogle ScholarPubMed
Salas-Huetos, A, Blanco, J, Vidal, F, Mercader, JM, Garrido, N, Anton, E. New insights into the expression profile and function of micro-ribonucleic acid in human spermatozoa. Fertil Steril. 2014;102(1):213–222.CrossRefGoogle ScholarPubMed
Grivna, ST, Beyret, E, Wang, Z, Lin, H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 2006;20(13):1709–1714.CrossRefGoogle ScholarPubMed
He, Z, Kokkinaki, M, Pant, D, Gallicano, GI, Dym, M. Small RNA molecules in the regulation of spermatogenesis. Reproduction. 2009;137(6):901–911.CrossRefGoogle ScholarPubMed
Wang, J, Zhang, P, Lu, Y, et al. PiRBase: a comprehensive database of piRNA sequences. Nucleic Acids Res. 2019;47(D1):D175–D180.CrossRefGoogle ScholarPubMed
Krawetz, SA, Kruger, A, Lalancette, C, et al. A survey of small RNAs in human sperm. Hum Reprod. 2011;26(12):3401–3412.Google Scholar
Pedroso Ayub, AL, D’Angelo Papaiz, D, da Silva Soares, R, Galvonas, JM. The function of lncRNAs as epigenetic regulators. In: Tutar, L, Aras, S, Tutar, E, eds. Non-Coding RNAs. IntechOpen; 2020:1–20.Google Scholar
Zhang, X, Gao, F, Fu, J, Zhang, P, Wang, Y, Zeng, X. Systematic identification and characterization of long non-coding RNAs in mouse mature sperm. PLoS ONE. 2017;12(3):e0173402.CrossRefGoogle ScholarPubMed
Dahariya, S, Paddibhatla, I, Kumar, S, Raghuwanshi, S, Pallepati, A, Gutti, RK. Long non-coding RNA: classification, biogenesis and functions in blood cells. Mol Immunol. 2019;112:82–92.CrossRefGoogle ScholarPubMed
Volders, PJ, Anckaert, J, Verheggen, K, et al. Lncipedia 5: towards a reference set of human long non-coding RNAs. Nucleic Acids Res. 2019;47(D1):D135–D139.Google Scholar
Zhang, X, Zhang, P, Song, D, et al. Expression profiles and characteristics of human lncRNA in normal and asthenozoospermia sperm. Biol Reprod. 2019;100(4):982–993.CrossRefGoogle ScholarPubMed
Zhu, L, Ge, J, Li, T, Shen, Y, Guo, J. tRNA-derived fragments and tRNA halves: the new players in cancers. Cancer Lett [Internet]. 2019;452:31–37. Available from: doi.org/10.1016/j.canlet.2019.03.012CrossRefGoogle ScholarPubMed
Kumar, P, Kuscu, C, Dutta, A. Biogenesis and function of transfer RNA related fragments (tRFs). Trends Biochem Sci. 2016;41(8):679–689.Google Scholar
Pliatsika, V, Loher, P, Magee, R, et al. MINTbase v2.0: a comprehensive database for tRNA-derived fragments that includes nuclear and mitochondrial fragments from all the Cancer Genome Atlas projects. Nucleic Acids Res. 2018;46(D1):D152–D159.Google Scholar
Hua, M, Liu, W, Chen, Y, et al. Identification of small non-coding RNAs as sperm quality biomarkers for in vitro fertilization. Cell Discov. 2019;5(1):20.Google Scholar
Trigg, NA, Eamens, AL, Nixon, B. The contribution of epididymosomes to the sperm small RNA profile. Reproduction. 2019;157:R209–R223.Google Scholar
Beard, JR, Officer, A, De Carvalho, IA, et al. The world report on ageing and health: a policy framework for healthy ageing. Lancet. 2016;387(10033):2145–2154.Google Scholar
Levine, H, Jørgensen, N, Martino-Andrade, A, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017;23(6):646–659.Google Scholar
Vollset, SE, Goren, E, Yuan, C, et al. Fertility, mortality, migration, and population scenarios for 195 countries and territories from 2017 to 2100: a forecasting analysis for the Global Burden of Disease Study. Lancet. 2020;396(10258):1285–1306.Google Scholar
Jenkins, TG, Aston, KI, Pflueger, C, Cairns, BR, Carrell, DT. Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLoS Genet. 2014;10(7):e1004458.Google Scholar
Jenkins, TG, James, ER, Aston, KI, et al. Age‑associated sperm DNA methylation patterns do not directly persist trans‑generationally. Epigenetics Chromatin. 2019;12:74.Google Scholar
Salas-Huetos, A, Blanco, J, Vidal, F, et al. Spermatozoa from patients with seminal alterations exhibit a differential micro-ribonucleic acid profile. Fertil Steril. 2015;104(3):591–601.CrossRefGoogle ScholarPubMed
Bhaskaran, K, Douglas, I, Forbes, H, Dos-Santos-Silva, I, Leon, DA, Smeeth, L. Body-mass index and risk of 22 specific cancers: a population-based cohort study of 5·24 million UK adults. Lancet. 2014;384(9945):755–765.Google Scholar
Salas-Huetos, A, Maghsoumi-Norouzabad, L, James, ER, et al. Male adiposity, sperm parameters and reproductive hormones: an updated systematic review and collaborative meta-analysis. Obes Rev. 2021;22(1):e13082.Google Scholar
Craig, JR, Jenkins, TG, Carrell, DT, Hotaling, JM. Obesity, male infertility, and the sperm epigenome. Fertil Steril. 2017;107(4):848–859.Google Scholar
Soubry, A, Guo, L, Huang, Z, et al. Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study. Clin Epigenetics. 2016;8(1):1–11.Google Scholar
Fullston, T, Ohlsson Teague, EMC, Palmer, NO, et al. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013;27(10):4226–4243.Google Scholar
Merzenich, H, Zeeb, H, Blettner, M. Decreasing sperm quality: a global problem? BMC Public Health. 2010;10(24):1–5.Google Scholar
Salas-Huetos, A, Bulló, M, Salas-Salvadó, J. Dietary patterns, foods and nutrients in male fertility parameters and fecundability: a systematic review of observational studies. Hum Reprod Update. 2017;23(4):371–389.CrossRefGoogle ScholarPubMed
Gaskins, AJ, Chavarro, JE. Diet and fertility: a review. Am J Obstet Gynecol. 2017;218(4):379–389.Google Scholar
Salas-Huetos, A, Rosique-Esteban, N, Becerra-Tomás, N, Vizmanos, B, Bulló, M, Salas-Salvadó, J. The effect of nutrients and dietary supplements on sperm quality parameters: a systematic review and meta-analysis of randomized clinical trials. Adv Nutr An Int Rev J. 2018;9(6):833–848.Google Scholar
Salas-Huetos, A, Babio, N, Carrell, DT, Bulló, M, Salas-Salvadó, J. Adherence to the Mediterranean diet is positively associated with sperm motility: a cross-sectional analysis. Sci Rep. 2019;9(1):3389.CrossRefGoogle Scholar
Xue, J, Gharaibeh, RZ, Pietryk, EW, et al. Impact of vitamin D depletion during development on mouse sperm DNA methylation. Epigenetics. 2018;13(9):959–974.Google Scholar
Lambrot, R, Xu, C, Saint-Phar, S, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4:2889.CrossRefGoogle ScholarPubMed
Chan, D, McGraw, S, Klein, K, et al. Stability of the human sperm DNA methylome to folic acid fortification and short-term supplementation. Hum Reprod. 2017;32(2):272–283.CrossRefGoogle ScholarPubMed
Aarabi, M, Christensen, KE, Chan, D, et al. Testicular MTHFR deficiency may explain sperm DNA hypomethylation associated with high dose folic acid supplementation. Hum Mol Genet. 2018;27(7):1123–1135.Google Scholar
Aarabi, M, San Gabrie, MC, Chan, D, et al. High-dose folic acid supplementation alters the human sperm methylome and is influenced by the MTHFR C677T polymorphism. Hum Mol Genet. 2015;24(22):6301–6313.Google Scholar
Watkins, AJ, Dias, I, Tsuro, H, et al. Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc Natl Acad Sci U S A. 2018;115(40):10064–10069.Google Scholar
Claycombe-Larson, KG, Bundy, AN, Roemmich, JN. Paternal high-fat diet and exercise regulate sperm miRNA and histone methylation to modify placental inflammation, nutrient transporter mRNA expression and fetal weight in a sex-dependent manner. J Nutr Biochem. 2020;81:108373.CrossRefGoogle Scholar
Nätt, D, Kugelberg, U, Casas, E, et al. Human sperm displays rapid responses to diet. PLoS Biol. 2019;17(12):e3000559.Google Scholar
Salas-Huetos, A, Moraleda, R, Giardina, S, et al. Effect of nut consumption on semen quality and functionality in healthy men consuming a Western-style diet: a randomized controlled trial. Am J Clin Nutr. 2018;108(5):953–962.Google Scholar
Sharma, R, Harlev, A, Agarwal, A, Esteves, SC. 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. 2016;70(4):635–645.Google Scholar
Marczylo, EL, Amoako, AA, Konje, JC, Gant, TW, Marczylo, TH. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics. 2012;7(5):432–439.CrossRefGoogle ScholarPubMed
Hamad, MF, Dayyih, WAA, Laqqan, M, AlKhaled, Y, Montenarh, M, Hammadeh, ME. The status of global DNA methylation in the spermatozoa of smokers and non-smokers. Reprod Biomed Online. 2018;37(5):581–589.Google Scholar
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;50(4):e12950.Google Scholar
Jenkins, TG, James, ER, Alonso, DF, et al. Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology. 2017;5(6):1089–1099.CrossRefGoogle ScholarPubMed
Murphy, PJ, Guo, J, Jenkins, TG, et al. NRF2 loss recapitulates heritable impacts of paternal cigarette smoke exposure. PLoS Genet. 2020;16(6):e1008756.Google Scholar

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