The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction

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Abstract

It is well-established that testicular spermatozoa are immature and acquire motility and fertilization capabilities during transit throughout the epididymis. The epididymis is a duct-like organ that connects the testis to the vas deferens and is comprised of four anatomical regions: the initial segment, caput, corpus, and cauda. Sperm maturation occurs during epididymal transit by the interaction of sperm cells with the unique luminal environment of each epididymal region. In this review we discuss the epididymis as an essential reproductive organ responsible for sperm concentration, maturation (including sperm motility acquisition and fertilizing ability), protection and storage. Importantly, we also discuss specific characteristics and roles of epididymal-derived exosomes (epididymosomes) in establishing sperm competency within the intricate process of reproduction. This review suggests that an increasing body of evidence is working to develop a complete picture of the role of the epididymis in male reproduction, offspring health, and disease susceptibility.

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Overview of Extracellular Vesicles, Their Origin, Composition, Purpose, and Methods for Exosome Isolation and Analysis

Laura M. Doyle, Michael Zhuo Wang (2019)

The use of extracellular vesicles, specifically exosomes, as carriers of biomarkers in extracellular spaces has been well demonstrated. Despite their promising potential, the use of exosomes in the clinical setting is restricted due to the lack of standardization in exosome isolation and analysis methods. The purpose of this review is to not only introduce the different types of extracellular vesicles but also to summarize their differences and similarities, and discuss different methods of exosome isolation and analysis currently used. A thorough understanding of the isolation and analysis methods currently being used could lead to some standardization in the field of exosomal research, allowing the use of exosomes in the clinical setting to become a reality.

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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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Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress.

Ali Rodgers, Christopher Morgan, N. Leu … (2015)

Epigenetic signatures in germ cells, capable of both responding to the parental environment and shaping offspring neurodevelopment, are uniquely positioned to mediate transgenerational outcomes. However, molecular mechanisms by which these marks may communicate experience-dependent information across generations are currently unknown. In our model of chronic paternal stress, we previously identified nine microRNAs (miRs) that were increased in the sperm of stressed sires and associated with reduced hypothalamic-pituitary-adrenal (HPA) stress axis reactivity in offspring. In the current study, we rigorously examine the hypothesis that these sperm miRs function postfertilization to alter offspring stress responsivity and, using zygote microinjection of the nine specific miRs, demonstrated a remarkable recapitulation of the offspring stress dysregulation phenotype. Further, we associated long-term reprogramming of the hypothalamic transcriptome with HPA axis dysfunction, noting a marked decreased in the expression of extracellular matrix and collagen gene sets that may reflect an underlying change in blood-brain barrier permeability. We conclude by investigating the developmental impact of sperm miRs in early zygotes with single-cell amplification technology, identifying the targeted degradation of stored maternal mRNA transcripts including sirtuin 1 and ubiquitin protein ligase E3a, two genes with established function in chromatin remodeling, and this potent regulatory function of miRs postfertilization likely initiates a cascade of molecular events that eventually alters stress reactivity. Overall, these findings demonstrate a clear mechanistic role for sperm miRs in the transgenerational transmission of paternal lifetime experiences.

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Journal

Journal ID (nlm-ta): Int J Mol Sci

Journal ID (iso-abbrev): Int J Mol Sci

Journal ID (publisher-id): ijms

Title: International Journal of Molecular Sciences

Publisher: MDPI

ISSN (Electronic): 1422-0067

Publication date (Electronic): 29 July 2020

Publication date Collection: August 2020

Volume: 21

Issue: 15

Electronic Location Identifier: 5377

Affiliations

[1 ]Andrology and IVF Laboratory, Division of Urology, Department of Surgery, University of Utah School of Medicine, Salt Lake City, UT 84108, USA; emma.james@ 123456utah.edu (E.R.J.); douglas.carrell@ 123456hsc.utah.edu (D.T.C.); ki.aston@ 123456hsc.utah.edu (K.I.A.)

[2 ]Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, UT 84112, USA

[3 ]Department of Physiology and Developmental Biology, Brigham Young University, Provo, UT 84604, USA; tim_jenkins@ 123456byu.edu

[4 ]Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Faculty of Sciences, Institute of Food and Agricultural Technology, University of Girona, 17003 Girona, Spain; marc.yeste@ 123456udg.edu

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[* ]Correspondence: albert.salas@ 123456utah.edu ; Tel.: +1-(385)-210-5534

Author information

Emma R. James https://orcid.org/0000-0001-5680-2131

Marc Yeste https://orcid.org/0000-0002-2209-340X

Albert Salas-Huetos https://orcid.org/0000-0001-5914-6862

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Publisher ID: ijms-21-05377

DOI: 10.3390/ijms21155377

PMC ID: 7432785

PubMed ID: 32751076

SO-VID: 0d784d84-e6b8-46df-b807-8c750c58a570

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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/).

The Role of the Epididymis and the Contribution of Epididymosomes to Mammalian Reproduction

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Bioscientifica Reproduction

Most cited references 73

Overview of Extracellular Vesicles, Their Origin, Composition, Purpose, and Methods for Exosome Isolation and Analysis

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

Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress.

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