Sperm epigenetics and influence of environmental factors

Ida Donkin, Romain Barrès, Ida Donkin, Romain Barrès

Abstract

Background: Developmental programming of the embryo is controlled by genetic information but also dictated by epigenetic information contained in spermatozoa. Lifestyle and environmental factors not only influence health in one individual but can also affect the phenotype of the following generations. This is mediated via epigenetic inheritance i.e., gametic transmission of environmentally-driven epigenetic information to the offspring. Evidence is accumulating that preconceptional exposure to certain lifestyle and environmental factors, such as diet, physical activity, and smoking, affects the phenotype of the next generation through remodeling of the epigenetic blueprint of spermatozoa.

Scope of review: This review will summarize current knowledge about the different epigenetic signals in sperm that are responsive to environmental and lifestyle factors and are capable of affecting embryonic development and the phenotype of the offspring later in life.

Major conclusions: Like somatic cells, the epigenome of spermatozoa has proven to be dynamically reactive to a wide variety of environmental and lifestyle stressors. The functional consequence on embryogenesis and phenotype of the next generation remains largely unknown. However, strong evidence of environmentally-driven sperm-borne epigenetic factors, which are capable of altering the phenotype of the next generation, is emerging on a large scale.

Keywords: DNA methylation; Epigenetic; Epigenetic inheritance; Histone; Small RNA; Sperm; Spermatozoa.

Copyright © 2018 The Authors. Published by Elsevier GmbH.. All rights reserved.

Figures

Figure 1
Figure 1
Lifestyle and environmental influences across generations. Exercise in the F0 generation may induce epigenetic reprogramming of the oocyte (1), and/or change whole body physiology (2) which, if still persistent when a pregnancy occurs, may have consequences on the extracellular milieu in utero (3). The developing embryo could be exposed to the exercise effects, thereby affecting not only the F1 (the embryo itself) but also the primordial germ cells developing in the embryo. Primordial germ cells represent, in part, the second-generation offspring, or F2. Exercise in the F0 may also alter behavior and metabolism in the F1 to influence aerobic capacity or inclination to exercise in the F1, which in turn induces programming of the spermatozoa through serial programming. Alternatively, exercise in the F0 may stably reprogram gametes throughout generations (F0, F1, … ), leading to true transgenerational epigenetic inheritance. Likely, the F2 generation is an integration of all epigenetic reprogramming that occurs throughout ancestors.
Figure 2
Figure 2
Overview of epigenetic marks susceptible to be remodeled with environmental insult. A simplified secondary structure of the sperm genome is represented, with the histone-bound DNA fraction accounting for less than 15% of the genome. DNA methylation remodeling is enhanced at CG rich, histone-bound fractions in sperm and is also found at repetitive elements. The positioning of histone relative to protamines may also be regulated by environmental factors. Histone modifications at specific loci are also changed after nutritional stress. Expression of small RNA (sRNA) such as tRNA fragments (tRF), microRNA (miRNA) and PIWI-interacting RNA (piRNA) is affected by lifestyle or environmental stress.

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