Oxidation of Sperm Nucleus in Mammals: A Physiological Necessity to Some Extent with Adverse Impacts on Oocyte and Offspring

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Abstract

Sperm cells have long been known to be good producers of reactive oxygen species, while they are also known to be particularly sensitive to oxidative damage affecting their structures and functions. As with all organic cellular components, sperm nuclear components and, in particular, nucleic acids undergo oxidative alterations that have recently been shown to be commonly encountered in clinical practice. This review will attempt to provide an overview of this situation. After a brief coverage of the biological reasons why the sperm nucleus and associated DNA are sensitive to oxidative damage, a summary of the most recent results concerning the oxidation of sperm DNA in animal and human models will be presented. The study will then attempt to cover the possible consequences of sperm nuclear oxidation on male fertility and beyond.

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Most cited references 43

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Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.

Q. Chen, M. Yan, Z. Cao … (2016)

Increasing evidence indicates that metabolic disorders in offspring can result from the father's diet, but the mechanism remains unclear. In a paternal mouse model given a high-fat diet (HFD), we showed that a subset of sperm transfer RNA-derived small RNAs (tsRNAs), mainly from 5' transfer RNA halves and ranging in size from 30 to 34 nucleotides, exhibited changes in expression profiles and RNA modifications. Injection of sperm tsRNA fractions from HFD males into normal zygotes generated metabolic disorders in the F1 offspring and altered gene expression of metabolic pathways in early embryos and islets of F1 offspring, which was unrelated to DNA methylation at CpG-enriched regions. Hence, sperm tsRNAs represent a paternal epigenetic factor that may mediate intergenerational inheritance of diet-induced metabolic disorders.

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Polyunsaturated fatty acids in male and female reproduction.

D Abayasekara, D. C. Wathes, R. Alan Aitken (2007)

In Westernized societies, average consumption of n-6 polyunsaturated fatty acids (PUFAs) far exceeds nutritional requirements. The ratio of n-6 to n-3 PUFAs is generally >10:1 whereas on a primitive human diet it was closer to 1:1. Diets fed to intensively farmed livestock have followed a similar trend. Both n-6 and n-3 PUFAs can influence reproductive processes through a variety of mechanisms. They provide the precursors for prostaglandin synthesis and can modulate the expression patterns of many key enzymes involved in both prostaglandin and steroid metabolism. They are essential components of all cell membranes. The proportions of different PUFAs in tissues of the reproductive tract reflect dietary consumption. PUFA supplements (particularly n-3 PUFAs in fish oil) are promoted for general health reasons. Fish oils may also benefit fertility in cattle and reduce the risk of preterm labor in women, but in both cases current evidence to support this is inconclusive. Gamma-linolenic acid containing oils can alter the types of prostaglandins produced by cells in vitro, but published data to support claims relating to effects on reproductive health are lacking. Spermatozoa require a high PUFA content to provide the plasma membrane with the fluidity essential at fertilization. However, this makes spermatozoa particularly vulnerable to attack by reactive oxygen species, and lifestyle factors promoting oxidative stress have clear associations with reduced fertility. Adequately powered trials that control for the ratios of different PUFAs consumed are required to determine the extent to which this aspect of our diets does influence our fertility.

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Oxidative stress, DNA methylation and carcinogenesis.

Rodrigo Franco, Onard JLM Schoneveld, Alexandros G. Georgakilas … (2008)

Transformation of a normal cell to a malignant one requires phenotypic changes often associated with each of the initiation, promotion and progression phases of the carcinogenic process. Genes in each of these phases acquire alterations in their transcriptional activity that are associated either with hypermethylation-induced transcriptional repression (in the case of tumor suppressor genes) or hypomethylation-induced activation (in the case of oncogenes). Growing evidence supports a role of ROS-induced generation of oxidative stress in these epigenetic processes and as such we can hypothesize of potential mode(s) of action by which oxidative stress modulates epigenetic regulation of gene expression. This is of outmost importance given that various components of the epigenetic pathway and primarily aberrant DNA methylation patterns are used as potential biomarkers for cancer diagnosis and prognosis.

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Journal

Journal ID (nlm-ta): Antioxidants (Basel)

Journal ID (iso-abbrev): Antioxidants (Basel)

Journal ID (publisher-id): antioxidants

Title: Antioxidants

Publisher: MDPI

ISSN (Electronic): 2076-3921

Publication date (Electronic): 23 January 2020

Publication date Collection: February 2020

Volume: 9

Issue: 2

Electronic Location Identifier: 95

Affiliations

[1 ]Faculty of Medicine, GReD Institute, INSERM U1103—CNRS UMR6293—Université Clermont Auvergne, CRBC building, 28 place Henri Dunant, 63001 Clermont-Ferrand, France

[2 ]School of Environmental and Life Sciences, Priority Research Centre for Reproductive Sciences, The University of Newcastle, Callaghan, Newcastle 2308, Australia; john.aitken@ 123456newcastle.edu.au

[3 ]Faculty of Health and Medicine, The University of Newcastle, Callaghan, Newcastle 2308, Australia

[4 ]Medical Genetics, Hunter Medical Research Institute, New Lambton Heights, 13 2305 Newcastle, Australia

Author notes

[* ]Correspondence: joel.drevet@ 123456uca.fr ; Tel.: +33-473407413

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Joël R. Drevet https://orcid.org/0000-0003-3077-6558

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Publisher ID: antioxidants-09-00095

DOI: 10.3390/antiox9020095

PMC ID: 7070651

PubMed ID: 31979208

SO-VID: 04b77e88-cd0b-4f65-b6f6-ce994addd124

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

Oxidation of Sperm Nucleus in Mammals: A Physiological Necessity to Some Extent with Adverse Impacts on Oocyte and Offspring

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Most cited references 43

Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder.

Polyunsaturated fatty acids in male and female reproduction.

Oxidative stress, DNA methylation and carcinogenesis.

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