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Extracellular Vesicles in Reproduction

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Biology".

Deadline for manuscript submissions: closed (31 October 2020) | Viewed by 79033

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Prof. Dr. Heriberto Rodriguez-Martinez

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Department of Clinical and Experimental Medicine, Faculty of Medicine and Health Sciences, Linköping University, SE-58185 Linköping, Sweden
Interests: andrology; reproductive biotechnologies; gamete interactions
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Prof. Dr. Jordi Roca

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Department of Medicine and Animal Surgery, Faculty of Veterinary Science, University of Murcia, Campus de Espinardo, 30100 Murcia, Spain
Interests: spermatozoa; seminal plasma; extracellular vesicles; proteomics; cytokines
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Prof. Dr. Emilio A. Martinez

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Department of Animal Medicine and Surgery, Faculty of Veterinary, University of Murcia, 30100 Murcia, Spain
Interests: animal reproduction
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Dear Colleagues,

The homeostasis of an individual depends basically on the ability of the differences cells, systems, and body compartments to interact via complex processes of communication. Among these, we know of humoral, hormonal, and nervous processes, and from the initial findings from the 1960s to today we include the role of cell-derived vesicles that communicate cell-to-cell beyond intercellular organized contacts, and vesicles that circulate in intercellular matrixes and secretions, lymph fluid, or blood to gain contact and mediate stimulus and responses at long distances from the originating cell. These extracellular vesicles (EVs) are further distinguished as exosomes, microvesicles, or apoptotic bodies, the latter being mostly related to cell death and nearby, local contacts, while the first names are related to systemic cell communication. All EVs have in common that they carry loads of molecules (proteins, peptides, lipids, carbohydrates, and nucleic acids) or even organelles (apoptotic bodies) with the capacity of respond to stimuli, intervene in metabolic pathways, or influence gene expression. Often having the characteristics of the originating cell, they serve as biomarkers of origin and of function beyond a specific target. The reproductive system is able to communicate via EVs, with some EVs playing important roles in spermatogenesis, sperm maturation, oogenesis, and embryogenesis, as well as influencing other systems, including the immune system to modulate immune responses, during the development and function of hemi-allogeneic organs as the placenta or the survival of the foetus throughout pregnancy.

This Issue of IJMS is focused on "Extracellular Vesicles in Reproduction”. The Issue welcomes papers covering EVs characterization, quantification, disclosure of their load, and elucidation of their biogenesis and roles when modulating reproductive events. The Issue welcomes novel research, certainly of comparative aspects but also of methodological papers, as well as insightful, critical reviews in these areas.

Prof. Dr. Heriberto Rodriguez-Martinez
Prof. Dr. Jordi Roca
Prof. Dr. Emilio A. Martinez
Guest Editors

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Keywords

extracellular vesicles
exosomes
microvesicles
apoptotic bodies
reproductive processes
spermatogenesis
sperm maturation
seminal plasma
spermatozoa
sperm capacitation
fertility
pregnancy
immune modulation
immune tolerance
proteomics
transcriptomics
epigenomics
metabolomics

Related Special Issues

Extracellular Vesicles in Reproduction 2.0 in International Journal of Molecular Sciences (6 articles)
Extracellular Vesicles in Reproduction 3.0 in International Journal of Molecular Sciences (2 articles)

Published Papers (13 papers)

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Research

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29 pages, 4797 KiB

Open AccessArticle

Isolation and Characterization of Equine Uterine Extracellular Vesicles: A Comparative Methodological Study

by Carmen Almiñana, Alba Rudolf Vegas, Muhittin Tekin, Mubbashar Hassan, Rustem Uzbekov, Thomas Fröhlich, Heinrich Bollwein and Stefan Bauersachs

Int. J. Mol. Sci. 2021, 22(2), 979; https://doi.org/10.3390/ijms22020979 - 19 Jan 2021

Cited by 19 | Viewed by 4182

Abstract

Extracellular vesicles (EVs) have been identified in the uterine fluid in different species and have been pointed as key players in the embryo-maternal dialogue, maternal recognition of pregnancy and establishment of pregnancy. However, little is known about the uterine EVs in the mare. Therefore, the present study aimed at characterizing EVs from uterine lavage of cyclic mares by comparing five EVs isolation methods and the combination of them: (1) ultracentrifugation (UC); (2) concentration of lavage volume by Centricon ultrafiltration (CE); (3) the use of CE with different washing steps (phosphate-buffered saline with or without trehalose); (4) size-exclusion chromatography with iZON-qEV columns, and (5) a combination of the methods with best results based on EVs yield, purity, and protein cargo profiles. Transmission electron microscopy and Western blotting confirmed the isolation of EVs by all methods but with quantitative and qualitative differences. Mass spectrometry provided differences in protein profiles between methods, number of identified proteins, and protein classes. Our results indicate that the combination of CE/trehalose/iZON/UC is an optimal method to isolate equine uterine EVs with good yield and purity that can be applied in future studies to determine the role of equine uterine EVs in embryo-maternal interactions. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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15 pages, 4026 KiB

Open AccessArticle

Extracellular Vesicles from Follicular and Ampullary Fluid Isolated by Density Gradient Ultracentrifugation Improve Bovine Embryo Development and Quality

by Anise Asaadi, Nima Azari Dolatabad, Hadi Atashi, Annelies Raes, Petra Van Damme, Michael Hoelker, An Hendrix, Osvaldo Bogado Pascottini, Ann Van Soom, Mojtaba Kafi and Krishna Chaitanya Pavani

Int. J. Mol. Sci. 2021, 22(2), 578; https://doi.org/10.3390/ijms22020578 - 8 Jan 2021

Cited by 29 | Viewed by 4722

Abstract

Extracellular vesicles (EVs) have been isolated from follicular (FF) and ampullary oviduct fluid (AOF), using different isolation methods. However, it is not clear whether different purification methods can affect the functionality of resulting EVs. Here, we compared two methods (OptiPrep™ density gradient ultracentrifugation (ODG UC) and single-step size exclusion chromatography (SEC) (qEV IZON™ single column)) for the isolation of EVs from bovine FF and AOF. Additionally, we evaluated whether the addition of EVs derived either by ODG UC or SEC from FF or AOF during oocyte maturation would yield extra benefits for embryo developmental competence. The characterization of EVs isolated using ODG UC or SEC from FF and AOF did not show any differences in terms of EV sizes (40–400 nm) and concentrations (2.4 ± 0.2 × 10¹²−1.8 ± 0.2 × 10¹³ particles/mL). Blastocyst yield and quality was higher in groups supplemented with EVs isolated from FF and AOF by ODG UC, with higher total cell numbers and a lower apoptotic cell ratio compared with the other groups (p < 0.05). Supplementing in vitro maturation media with EVs derived by ODG UC from AOF was beneficial for bovine embryo development and quality. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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17 pages, 1581 KiB

Open AccessArticle

MicroRNAs from Extracellular Vesicles Secreted by Bovine Embryos as Early Biomarkers of Developmental Competence

by Bárbara Melo-Baez, Yat S. Wong, Constanza J. Aguilera, Joel Cabezas, Ana C. F. Mançanares, Gonzalo Riadi, Fidel O. Castro and Lleretny Rodriguez-Alvarez

Int. J. Mol. Sci. 2020, 21(23), 8888; https://doi.org/10.3390/ijms21238888 - 24 Nov 2020

Cited by 18 | Viewed by 2657

Abstract

During early development, embryos secrete extracellular vesicles (EVs) that participate in embryo–maternal communication. Among other molecules, EVs carry microRNAs (miRNAs) that interfere with gene expression in target cells; miRNAs participate in embryo–maternal communication. Embryo selection based on secreted miRNAs may have an impact on bovine breeding programs. This research aimed to evaluate the size, concentration, and miRNA content of EVs secreted by bovine embryos with different developmental potential, during the compaction period (days 3.5–5). Individual culture media from in vitro–produced embryos were collected at day 5, while embryos were further cultured and classified at day 7, as G1 (conditioned-culture media by embryos arrested in the 8–16-cells stage) and G2 (conditioned-culture media by embryos that reached blastocyst stages at day 7). Collected nanoparticles from embryo conditioned culture media were cataloged as EVs by their morphology and the presence of classical molecular markers. Size and concentration of EVs from G1 were higher than EVs secreted by G2. We identified 95 miRNAs; bta-miR-103, bta-miR-502a, bta-miR-100, and bta-miR-1 were upregulated in G1, whereas bta-miR-92a, bta-miR-140, bta-miR-2285a, and bta-miR-222 were downregulated. The most significant upregulated pathways were fatty acid biosynthesis and metabolism, lysine degradation, gap junction, and signaling pathways regulating pluripotency of stem cells. The characteristics of EVs secreted by bovine embryos during the compaction period vary according to embryo competence. Embryos that reach the blastocyst stage secrete fewer and smaller vesicles. Furthermore, the loading of specific miRNAs into the EVs depends on embryo developmental competence. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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19 pages, 5157 KiB

Open AccessArticle

Proteomic Profiling of Two Distinct Populations of Extracellular Vesicles Isolated from Human Seminal Plasma

by Xiaogang Zhang, Harmjan R. Vos, Weiyang Tao and Willem Stoorvogel

Int. J. Mol. Sci. 2020, 21(21), 7957; https://doi.org/10.3390/ijms21217957 - 26 Oct 2020

Cited by 16 | Viewed by 3522

Abstract

Body fluids contain many populations of extracellular vesicles (EV) that differ in size, cellular origin, molecular composition, and biological activities. EV in seminal plasma are in majority originating from prostate epithelial cells, and hence are also referred to as prostasomes. Nevertheless, EV are also contributed by other accessory sex glands, as well as by the testis and epididymis. In a previous study, we isolated EV from seminal plasma of vasectomized men, thereby excluding contributions from the testis and epididymis, and identified two distinct EV populations with diameters of 50 and 100 nm, respectively. In the current study, we comprehensively analyzed the protein composition of these two EV populations using quantitative Liquid Chromatography-Mass Spectrometry (LC-MS/MS). In total 1558 proteins were identified. Of these, ≈45% was found only in the isolated 100 nm EV, 1% only in the isolated 50 nm EV, and 54% in both 100 nm and 50 nm EV. Gene ontology (GO) enrichment analysis suggest that both originate from the prostate, but with distinct biogenesis pathways. Finally, nine proteins, including KLK3, KLK2, MSMB, NEFH, PSCA, PABPC1, TGM4, ALOX15B, and ANO7, with known prostate specific expression and alternate expression levels in prostate cancer tissue were identified. These data have potential for the discovery of EV associated prostate cancer biomarkers in blood. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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16 pages, 2222 KiB

Open AccessArticle

Bovine Follicular Fluid and Extracellular Vesicles Derived from Follicular Fluid Alter the Bovine Oviductal Epithelial Cells Transcriptome

by Mohammad Mehedi Hasan, Janeli Viil, Freddy Lättekivi, James Ord, Qurat Ul Ain Reshi, Kersti Jääger, Agne Velthut-Meikas, Aneta Andronowska, Ülle Jaakma, Andres Salumets and Alireza Fazeli

Int. J. Mol. Sci. 2020, 21(15), 5365; https://doi.org/10.3390/ijms21155365 - 28 Jul 2020

Cited by 18 | Viewed by 4493

Abstract

While follicular fluid (FF) is well known to provide an optimal environment for oogenesis, its functional roles following its release into the oviduct during ovulation are currently elusive. We hypothesized that FF and FF-derived extracellular vesicles (EVs) may be conveyors of signals capable of inducing functionally-relevant transcriptional responses in oviductal cells. The aim of this study was, therefore, to evaluate the effect of FF and FF-derived EVs on the transcriptome of primary bovine oviductal epithelial cells (BOECs). We examined the gene expression of BOECs in three conditions: BOECs cultured with FF, FF-derived EVs, and without supplementations. For each condition, cells were cultured for 6 and 24 h. RNA sequencing results revealed that FF had a stronger effect on BOECs gene expression compared to EVs. We detected 488 and 1998 differentially expressed genes (DEGs) with FF treatment in 6 and 24 h, respectively, whereas only 41 DEGs were detected at 6 h following EV treatment. Pathway analysis of the FF-induced DEGs showed that several pathways were highly enriched, notably oxidative phosphorylation, thermogenesis, arachidonic acid metabolism, and steroid hormone biosynthesis. Some of these pathways have a role in sperm survival, fertilization, and early embryo development. In conclusion, the findings of our study demonstrate for the first time that bovine FF and FF-derived EVs can induce changes in the gene expression of the bovine oviductal cells which, although observed in vitro, may be reflective of in vivo responses which may contribute to a favorable periconceptional microenvironment for sperm survival, fertilization, and early embryo development. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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13 pages, 1884 KiB

Open AccessArticle

Oviduct Fluid Extracellular Vesicles Change the Phospholipid Composition of Bovine Embryos Developed In Vitro

by Charles Banliat, Daniel Le Bourhis, Ophélie Bernardi, Daniel Tomas, Valérie Labas, Pascal Salvetti, Benoît Guyonnet, Pascal Mermillod and Marie Saint-Dizier

Int. J. Mol. Sci. 2020, 21(15), 5326; https://doi.org/10.3390/ijms21155326 - 27 Jul 2020

Cited by 27 | Viewed by 2788

Abstract

Oviduct fluid extracellular vesicles (oEVs) have been proposed as bringing key molecules to the early developing embryo. In order to evaluate the changes induced by oEVs on embryo phospholipids, fresh bovine blastocysts developed in vitro in the presence or absence of oEVs were analyzed by intact cell MALDI-TOF (Matrix assisted laser desorption ionization—Time of flight) mass spectrometry (ICM-MS). The development rates, cryotolerance, and total cell number of blastocysts were also evaluated. The exposure to oEVs did not affect blastocyst yield or cryotolerance but modified the phospholipid content of blastocysts with specific changes before and after blastocoel expansion. The annotation of differential peaks due to oEV exposure evidenced a shift of embryo phospholipids toward more abundant phosphatidylcholines (PC), phosphatidylethanolamines (PE), and sphingomyelins (SM) with long-chain fatty acids. The lipidomic profiling of oEVs showed that 100% and 33% of the overabundant masses in blastocysts and expanded blastocysts, respectively, were also present in oEVs. In conclusion, this study provides the first analysis of the embryo lipidome regulated by oEVs. Exposure to oEVs induced significant changes in the phospholipid composition of resulting embryos, probably mediated by the incorporation of oEV-phospholipids into embryo membranes and by the modulation of the embryonic lipid metabolism by oEV molecular cargos. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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20 pages, 3508 KiB

Open AccessArticle

Oviductal Extracellular Vesicles Improve Post-Thaw Sperm Function in Red Wolves and Cheetahs

by Marcia de Almeida Monteiro Melo Ferraz, Jennifer Beth Nagashima, Michael James Noonan, Adrienne E. Crosier and Nucharin Songsasen

Int. J. Mol. Sci. 2020, 21(10), 3733; https://doi.org/10.3390/ijms21103733 - 25 May 2020

Cited by 21 | Viewed by 4407

Abstract

Artificial insemination (AI) is a valuable tool for ex situ wildlife conservation, allowing the re-infusion and dissemination of genetic material, even after death of the donor. However, the application of AI to species conservation is still limited, due mainly to the poor survival of cryopreserved sperm. Recent work demonstrated that oviductal extracellular vesicles (oEVs) improved cat sperm motility and reduced premature acrosomal exocytosis. Here, we build on these findings by describing the protein content of dog and cat oEVs and investigating whether the incubation of cryopreserved red wolf and cheetah sperm with oEVs during thawing improves sperm function. Both red wolf and cheetah sperm thawed with dog and cat oEVs, respectively, had more intact acrosomes than the non-EV controls. Moreover, red wolf sperm thawed in the presence of dog oEVs better maintained sperm motility over time (>15%) though such an improvement was not observed in cheetah sperm. Our work demonstrates that dog and cat oEVs carry proteins important for sperm function and improve post-thaw motility and/or acrosome integrity of red wolf and cheetah sperm in vitro. The findings show how oEVs can be a valuable tool for improving the success of AI with cryopreserved sperm in threatened species. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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12 pages, 2264 KiB

Open AccessCommunication

The Separation and Characterization of Extracellular Vesicles from Medium Conditioned by Bovine Embryos

by Krishna Chaitanya Pavani, Xiaoyuan Lin, Joachim Hamacher, Wim Van Den Broeck, Liesbeth Couck, Luc Peelman, An Hendrix and Ann Van Soom

Int. J. Mol. Sci. 2020, 21(8), 2942; https://doi.org/10.3390/ijms21082942 - 22 Apr 2020

Cited by 16 | Viewed by 4637

Abstract

Extracellular vesicles (EVs) have been identified as one of the communication mechanisms amongst embryos. They are secreted into the embryo culture medium and, as such, represent a source of novel biomarkers for identifying the quality of cells and embryos. However, only small amounts of embryo-conditioned medium are available, which represents a challenge for EV enrichment. Our aim is to assess the suitability of different EV separation methods to retrieve EVs with high specificity and sufficient efficiency. Bovine embryo-conditioned medium was subjected to differential ultracentrifugation (DU), OptiPrep^TM density gradient (ODG) centrifugation, and size exclusion chromatography. Separated EVs were characterized by complementary characterization methods, including Western blot, electron microscopy, and nanoparticle tracking analysis, to assess the efficiency and specificity. OptiPrep^TM density gradient centrifugation outperformed DU and SEC in terms of specificity by substantial removal of contaminating proteins such as ribonucleoprotein complexes (Argonaute-2 (AGO-2)) and lipoproteins (ApoA-I) from bovine embryo-derived EVs (density: 1.02–1.04, 1.20–1.23 g/mL, respectively). In conclusion, ODG centrifugation is the preferred method for identifying EV-enriched components and for improving our understanding of EV function in embryo quality and development. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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Review

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20 pages, 2786 KiB

Open AccessReview

Extracellular Vesicles and the Oviduct Function

by Emily A. Harris, Kalli K. Stephens and Wipawee Winuthayanon

Int. J. Mol. Sci. 2020, 21(21), 8280; https://doi.org/10.3390/ijms21218280 - 5 Nov 2020

Cited by 37 | Viewed by 5226

Abstract

In mammals, the oviduct (or the Fallopian tube in humans) can be divided into the infundibulum (responsible for oocyte pick-up), ampulla (site of fertilization), isthmus (where preimplantation embryos develop), and uterotubal junction (where embryos transit to the uterus). The oviductal fluid, as well as extracellular vesicles produced from the oviduct epithelial cells, referred to as oEVs, have been shown to improve the fertilization process, prevent polyspermy, and aid in embryo development. oEVs contain molecular cargos (such as miRNAs, mRNAs, proteins, and lipids) that can be delivered and fuse to recipient cells. oEVs produced from the ampulla appear to be functionally distinct from those produced from the isthmus. In multiple species including mice, cats, dogs, pigs, and cows, oEVs can be incorporated into the oocytes, sperm, and embryos. In this review, we show the positive impact of oEVs on gamete function as well as blastocyst development and how they may improve embryo quality in in vitro conditions in an assisted reproductive technology setting for rodents, domestic animals, farm animals, and humans. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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30 pages, 2238 KiB

Open AccessReview

Tetraspanins, More than Markers of Extracellular Vesicles in Reproduction

by Jana Jankovičová, Petra Sečová, Katarína Michalková and Jana Antalíková

Int. J. Mol. Sci. 2020, 21(20), 7568; https://doi.org/10.3390/ijms21207568 - 14 Oct 2020

Cited by 96 | Viewed by 6209

Abstract

The participation of extracellular vesicles in many cellular processes, including reproduction, is unquestionable. Although currently, the tetraspanin proteins found in extracellular vesicles are mostly applied as markers, increasing evidence points to their role in extracellular vesicle biogenesis, cargo selection, cell targeting, and cell uptake under both physiological and pathological conditions. In this review, we bring other insight into the involvement of tetraspanin proteins in extracellular vesicle physiology in mammalian reproduction. We provide knowledge regarding the involvement of extracellular vesicle tetraspanins in these processes in somatic cells. Furthermore, we discuss the future direction towards an understanding of their functions in the tissues and fluids of the mammalian reproductive system in gamete maturation, fertilization, and embryo development; their involvement in mutual cell contact and communication in their complexity. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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15 pages, 1073 KiB

Open AccessReview

Emerging Role of Extracellular Vesicles in Embryo–Maternal Communication throughout Implantation Processes

by Keigo Nakamura, Kazuya Kusama, Yoshihito Suda, Hiroshi Fujiwara, Masatoshi Hori and Kazuhiko Imakawa

Int. J. Mol. Sci. 2020, 21(15), 5523; https://doi.org/10.3390/ijms21155523 - 1 Aug 2020

Cited by 17 | Viewed by 4555

Abstract

In ruminants, the establishment of proper conceptus–endometrial communication is essential for conceptus implantation and subsequent successful placentation. Accumulated evidence supports the idea that extracellular vesicles (EVs) present in uterine lumen are involved in conceptus–endometrial interactions during the preimplantation period. EVs make up a new field of intercellular communicators, which transport a variety of bioactive molecules, including soluble and membrane-bound proteins, lipids, DNA, and RNAs. EVs thus regulate gene expression and elicit biological effects including increased cell proliferation, migration, and adhesion in recipient cells. Uterine EVs are interactive and coordinate with ovarian progesterone (P4), trophectoderm-derived interferon tau (IFNT) and/or prostaglandins (PGs) in the physiological or pathological microenvironment. In this review, we will focus on intrauterine EVs in embryo–maternal interactions during the early stage of pregnancy, especially the implantation period in ruminant ungulates. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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17 pages, 1024 KiB

Open AccessReview

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

by Emma R. James, Douglas T. Carrell, Kenneth I. Aston, Timothy G. Jenkins, Marc Yeste and Albert Salas-Huetos

Int. J. Mol. Sci. 2020, 21(15), 5377; https://doi.org/10.3390/ijms21155377 - 29 Jul 2020

Cited by 133 | Viewed by 21050

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. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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16 pages, 1651 KiB

Open AccessReview

Exosomes as Messengers between Mother and Fetus in Pregnancy

by Liliana Czernek and Markus Düchler

Int. J. Mol. Sci. 2020, 21(12), 4264; https://doi.org/10.3390/ijms21124264 - 15 Jun 2020

Cited by 77 | Viewed by 9320

Abstract

The ability of exosomes to transport different molecular cargoes and their ability to influence various physiological factors is already well known. An exciting area of research explores the functions of exosomes in healthy and pathological pregnancies. Placenta-derived exosomes were identified in the maternal circulation during pregnancy and their contribution in the crosstalk between mother and fetus are now starting to become defined. In this review, we will try to summarize actual knowledge about this topic and to answer the question of how important exosomes are for a healthy pregnancy. Full article

(This article belongs to the Special Issue Extracellular Vesicles in Reproduction)

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