Sperm interactions with the female reproductive tract: A key for successful fertilization in mammals

doi:10.1016/j.mce.2020.110956

Molecular and Cellular Endocrinology

Volume 516, 1 October 2020, 110956

https://doi.org/10.1016/j.mce.2020.110956 Get rights and content

Highlights

•
Sperm viability and capacitation imply cellular interactions in the female tract.
•
Female tract secretions have region- and stage-specific effects on sperm physiology.
•
A special attention is given on secreted proteins that modulate sperm physiology.
•
Oviductal extracellular vesicles appear to be key components of sperm capacitation.

Abstract

Sperm migration through the female genital tract is not a quiet journey. Uterine contractions quickly operate a drastic selection, leading to a very restrictive number of sperm reaching the top of uterine horns and finally, provided the presence of key molecules on sperm, the oviduct, where fertilization takes place. During hours and sometimes days before fertilization, subpopulations of spermatozoa interact with dynamic and region-specific maternal components, including soluble proteins, extracellular vesicles and epithelial cells lining the lumen of the female tract. Interactions with uterine and oviductal cells play important roles for sperm survival as they modulate the maternal immune response and allow a transient storage before ovulation. The body of work reported here highlights the importance of sperm interactions with proteins originated from both the uterine and oviductal fluids, as well as hormonal signals around the time of ovulation for sperm acquisition of fertilizing competence.

Introduction

Ejaculated mammalian spermatozoa are not able to fertilize the oocyte; this ability is acquired following a series of molecular and physiological changes, collectively known as capacitation, which are accomplished during the transit of spermatozoa through the female genital tract. In addition to sperm acquisition of fertilizing competence, the maternal environment operates a dramatic sperm selection, resulting in a very low sperm:egg ratio in the site of fertilization (Hino et al., 2016). The maternal environment allows also long-term survival of a subpopulation of spermatozoa up to the time of ovulation. These crucial steps preceding fertilization imply sperm interactions with the complex and dynamic fluids present in the female reproductive tract and with epithelial cells lining its lumen, in addition to flows induced by muscular contractions of the female genital tract. Fertilization can occur in vitro, thus in the absence of these interactions, but the female tract may increase the efficiency and quality of fertilization. To illustrate, the rate of polyspermy and the incidence of chromosomal abnormalities in early embryos are generally much lower in vivo than under in vitro conditions (Coy and Aviles, 2010; Viuff et al., 2000, 2001). Therefore, the mechanisms involved in sperm interactions with somatic cells and region-specific secretions in vivo are of particular importance for the understanding of factors determining male and female fertility, but also for the improvement of assisted reproductive technologies (ART) and for better evaluation/prediction of male fertility in human and farm animals.

The objective of this review is to provide an update on the effects of interactions in the uterus, utero-tubal junction (UTJ) and the oviduct (known as the fallopian tube in human) on sperm physiology, with emphasis on the oviduct where fertilization takes place. Physical and biochemical interactions of spermatozoa in the cervix have been recently reviewed (Fair et al., 2019; Rickard et al., 2019) and were not included. In each region starting from the uterus, effects of interaction with secreted fluids, including extracellular vesicles, and luminal epithelial cells on sperm will be considered separately. Special attention will be given to sperm-interacting proteins identified in female secretions that modulate sperm physiology. However, details on the reorganization of specific sperm surface microdomains and proteins during capacitation were excluded as they are well described elsewhere (Baker, 2016; Brohi and Huo, 2017; Gadella, 2017). The changes induced by sperm interactions on female tract gene expression were also considered out of the scope of the present review. All mammals will be considered with a particular interest in farm animals, in which large amounts of data on sperm interactions were acquired thanks to the availability of the biological material and due to the economic importance of such research area for animal breeding and livestock production.

Section snippets

Sperm interactions with the uterus

The migration of spermatozoa through the uterus is associated with sperm interactions with the uterine fluid (UF) and with uterine (or endometrial) epithelial cells (UECs), each mediated by specific components and triggering different effects on sperm.

Factors involved in sperm migration up to the utero-tubal junction

The migration of spermatozoa up to the oviduct is the result of a combination of several male and female parameters. As spermatozoa swim in the uterine fluid to reach the UTJ, sperm mobility and morphology are expected to be limiting factors of sperm migration. After intrauterine insemination in sows, an increase in the proportion of morphologically abnormal sperm collected in the backflow from uterus to vagina was observed while this proportion was lower among sperm recovered in the UTJ (

Sperm interactions with the oviduct

After mating or insemination, a very small proportion of spermatozoa reach the oviduct. Genital tracts collected after insemination in cows and gilts evidenced no more than a few dozens to hundreds of sperm within the oviduct (Hunter, 1981; Hunter et al., 1991; Hunter and Wilmut, 1984; Sostaric et al., 2008). As oviducts are small intra-abdominal organs not accessible on animals without surgery or slaughter, exact information on oviductal sperm behavior in vivo is scarce and most data were

Conclusions

The interactions taking place between spermatozoa and the female reproductive tract operate a drastic selection among male gametes, leading to a small subpopulation of top quality spermatozoa at the site of fertilization. Sperm selection involves uterine contractions to remove dead and abnormal spermatozoa from the uterus but also various mechanisms including sperm phagocytosis mediated by uterine inflammatory response, key molecules on sperm surface to cross the UTJ, binding to the oviductal

Acknowledgments

This work was funded by INRAe and Agence Nationale de la Recherche under the grant number ANR-18-CE92-0049. We thank Marc Chodkievicz for careful reading and edition of this manuscript. We thank Thierry Meylheuc, from the imaging facility at the microscopy and imaging platform MIMA2 (INRAe, Jouy-en-Josas, France), Maryse Meurisse and Marie-Claire Blache, from the microscopy and imaging platform PIC (INRAe, Nouzilly, France), for their help with scanning electronic and confocal microscopy

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The Syngnathidae (seahorses and pipefishes) are a group of teleost fishes in which, uniquely, developing embryos are hosted throughout pregnancy by males, using a specialized brood pouch situated on the abdomen or tail. Seahorses have evolved the most advanced form of brood pouch, whereby zygotes and embryos are intimately connected to the host’s circulatory system and also bathed in pouch fluid. The pouch is closed to the external environment and has to perform functions such as gaseous exchange, removal of waste and maintenance of appropriate osmotic conditions, much like the mammalian placenta. Fertilization of the oocytes occurs within the brood pouch, but unlike the mammalian situation the sperm transport mechanism from the ejaculatory duct towards the pouch is unclear, and the sperm: egg ratio (about 5:1) is possibly the least of any vertebrate. In this review, there is highlighting of the difficulty of elucidating the sperm transport mechanism, based on studies of Hippocampus kuda. The similarities between seahorse pouch function and the mammalian placenta have led to suggestions that the pouch provides important nutritional support for the developing embryos, supplementing the nutritional functions of the yolk sac provided by the oocytes. In this review, there is a description of the recent evidence in support of this hypothesis, and also emphasis, as in mammals, that embryonic development depends on nutritional support from the placenta-like pouch at important stages of the gestational period (“critical windows”).
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Sperm are held in the reservoir as a result of a binding interaction between ligands on the sperm head and receptors on the epithelium (Coy et al., 2012). There is evidence that formation of the reservoir serves to maintain a source of viable sperm in the oviduct until the time when ovulation occurs, as well as to prevent polyspermic fertilization by releasing sperm gradually from the reservoir (Suarez, 2016; Saint-Dizier et al., 2020). Results of experiments performed in vitro using explants or cultured monolayers of oviductal epithelium provide evidence that only motile, morphologically normal sperm that are not capacitated bind to the oviductal epithelium, indicating that binding is selective (Saint-Dizier et al., 2020).
Evaluation of sperm motility is well-established in farm animals for quickly selecting ejaculates for semen processing into insemination doses and for evaluating the quality of preserved semen. Likewise, sperm motility is a fundamental parameter used by spermatologists in basic and applied science. Motility is commonly assessed using computer-assisted semen analysis (CASA). Recent increases in computational power, as well as utilization of mobile CASA systems and open-source CASA programs, broaden the possibilities for motility evaluation. Despite this technological progress, the potential of computer-generated motility data to assess male fertility remains challenging and may be limited. Relevance for fertility assessment could be improved if measurement conditions would more closely mimic the in vivo situation. Hence, this review is focused on the current trends of automated semen assessment in livestock and explores perspectives for future use with respect to the physiological and physical conditions encountered by sperm in the female reproductive tract. Validation of current CASA systems with more complex, microfluidic-based devices mimicking the female reproductive tract environment could improve the value of sperm kinematic data for assessing the fertilizing capacity of semen samples, not only for application in livestock but also for use in conducting assisted reproduction techniques in other species.
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Sperm subpopulations are subsequently modified by the milieu of the female reproductive tract (both in external and internal fertilization), the interaction with the female reproductive tract (including attachment to the oviductal lining and analogous structures in the case of internal fertilization), and, of course, the application of assisted reproductive techniques (especially those related to sperm storage and cryostorage). Because the aim of this review is to reflect on the ultimate origin of the sperm subpopulations (which would condition the subpopulation structures subsequently emerging from these processes), the reader is encouraged to evaluate the rich literature base related to this fascinating topic (Santiago-Moreno et al., 2016; Yeste, 2016; Amann et al., 2018; Roldan, 2020; Saint-Dizier et al., 2020; Barquero et al., 2021). It is time that those conducting studies of the sperm subpopulations take advantage of new developments in sperm analysis.
The study of sperm subpopulations spans three decades. The origin, meaning, and practical significance, however, are less clear. Current technology for assessing sperm morphology (CASA-Morph) and motility (CASA-Mot) has enabled the accurate evaluation of these features, and there are many options for data classification. Subpopulations could occur as a result of the stage of development of each spermatozoon in the subpopulation. Spermatogenesis might contribute to the production of these subpopulations. Insights from evolutionary biology and recent molecular research are indicative of the diversity among male gametes that could occur from unequal sharing of transcripts and other elements through cytoplasmic bridges between spermatids. Sperm cohorts exiting the gonads would contain different RNA and protein contents, affecting the spermatozoon physiology and associations with the surrounding environmental milieu. Subsequently, these differences could affect how spermatozoa interact with the environmental milieu (maturation, mixing with seminal plasma, and interacting with the environmental milieu, or female genital tract and female gamete). The emergence of sperm subpopulations as an outcome of evolution, related to the reproductive strategies of the species, genital tract structures, and copulatory and fertilization processes. This kind of approach in determining the importance of sperm subpopulations in fertilization capacity should have a practical impact for conducting reproductive technologies, inspiring and enabling new ways for the more efficient use of spermatozoa in the medical, animal breeding, and conservation fields. This manuscript is a contribution to the Special Issue in memory of Dr. Duane Garner.
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These results suggest that uterosomes may play a role in sperm maturation and may even transmit their own material to the embryo, which is important for embryonic development and embryo-endometrial interactions. A comprehensive discussion on the interactions of sperm with the uterosomes and other cells/tissues in the female reproductive tract is beyond the aim of this paper (see [(Martin-DeLeon, 2016; Saint-Dizier et al., 2020)] for an overview). Sperm reach the uterus and may modify the genetic structure, as discussed in earlier sections. (
Telegony refers to the appearance of some characteristics of the female's previously mated male in her subsequent offspring by another male. According to evidence, telegony may occur either through the infiltration of sperm into the somatic tissues of the female genital tract or the presence of fetal genes in the mother's blood. It is highlighted that sperm penetrates into the mucosa of the uterine and possibly alters the genetic structure, affecting the embryo and enduring from one pregnancy to the next, which may be one of the potential mechanisms of telegony. Uterine fluid, uterine gland-derived histotroph, supplies key nutrients for successful embryo implantation and it is important during the first trimester, especially, because of its susceptibility to maternal states. The presence of EVs in uterine fluid (uterosomes) was reported in mice, sheep, and humans, including a wide range of biomolecules, such as proteins, and non-coding RNAs. In this review article, we presented a new idea to explain telegony. Based on our idea, after the previous male sperm entry into the female reproductive system, those sperm which do not participate in fertilization penetrate into the somatic cells of the uterus and store their genetic/epigenetic information there. The sperm of the next partner reaches a location in the female reproductive canal where it exchanges information with the uterosomes and obtains the proteins and non-coding RNAs required for fertilization, development, and implantation.
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Studies have shown that exosomes transport a variety of biomolecules, including lipids, proteins, receptors and effector molecules, to recipient cells [25,26]. Furthermore, there is increasing evidence showing that seminal plasma and extracellular vesicles (exosomes and microvesicles) are not only sperm carriers but also play a crucial role in other reproductive physiology activities [27]. Studies show that seminal plasma exosomes, which could alter the lipid composition of the sperm membrane, assist in the production of future sperm motility and the ability to penetrate the zona pellucida [17].
Multiple physiological pathways are controlled by exosomes. Exosomes may be found in seminal plasma where they carry functional molecules to the sperm, such as microRNAs (miRNAs). Sperm cytoplasmic droplets (CDs) are remnants of cytoplasm, and their migration is a morphological characteristic of epididymal maturation. However, miRNA expression patterns in seminal plasma exosomes found in semen containing spermatozoa with CDs versus regular exosomes in boar semen have not been examined. In this study, seminal plasma exosomes were isolated from semen containing spermatozoa with CDs and miRNA expression profiles were analyzed. A total of 348 known and 206 new miRNAs were identified. Sixteen miRNAs were significantly differentially expressed. Of these, 13 miRNAs (ssc-miR-101, ssc-miR-148a-5p, ssc-miR-184, ssc-miR-202–3p, ssc-miR-221–5p, ssc-miR-2483, ssc-miR-29a-3p, ssc-miR-29c, ssc-miR-31, ssc-miR-362, ssc-miR-500–5p, ssc-miR-542–3p, and ssc-miR-769–5p) were significantly upregulated, whereas three miRNAs (ssc-miR-1249, ssc-miR-155–5p, and ssc-miR-296–5p) were significantly downregulated. GO and KEGG pathway analyses showed that these targeted genes were enriched for functions such as metabolic process, reproductive process, proteasome, ubiquitin mediated proteolysis, and oxidative phosphorylation. Therefore, seminal plasma exosomes are predicted to play a key role in the regulation of sperm CDs.

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ReviewSperm interactions with the female reproductive tract: A key for successful fertilization in mammals

Highlights

Abstract

Introduction

Section snippets

Sperm interactions with the uterus

Factors involved in sperm migration up to the utero-tubal junction

Sperm interactions with the oviduct

Conclusions

Acknowledgments

Secretory products of bovine oviductal epithelial cells support the viability and motility of bovine spermatozoa in culture in vitro

J. Exp. Zool.

Bovine oviduct-specific glycoprotein: a potent factor for maintenance of viability and motility of bovine spermatozoa in vitro

Mol. Reprod. Dev.

Sperm enter glands of preovulatory bovine endometrial explants and initiate inflammation

Reproduction

Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm

PloS One

Oviductosome-sperm membrane interaction in cargo delivery: detection OF FUSION and underlying molecular players using three-dimensional super-resolution structured illumination microscopy (SR-SIM)

J. Biol. Chem.

Porcine oviductal extracellular vesicles interact with gametes and regulate sperm motility and survival

Theriogenology

Oviduct fluid extracellular vesicles regulate polyspermy during porcine in vitro fertilisation

Reprod. Fertil. Dev.

Oviduct fluid extracellular vesicles regulate polyspermy during porcine in vitro fertilization

Reprod. Fertil. Dev.

Seminal DNase frees spermatozoa entangled in neutrophil extracellular traps

Biol. Reprod.

Species-specific interaction of seminal plasma on sperm-neutrophil binding

Anim. Reprod. Sci.

Extracellular vesicles in the oviduct: progress, challenges and implications for the reproductive success

Bioengineering

Oviduct extracellular vesicles protein content and their role during oviduct-embryo cross-talk

Reproduction

Modulatory effects of bovine seminal plasma on uterine inflammatory processes

Reprod. in domes. animals Zuchthygiene

Effect of a null mutation of the oviduct-specific glycoprotein gene on mouse fertilization

Biochem. J.

Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo

Reproduction

Dynamics of bovine sperm interaction with epithelium differ between oviductal isthmus and ampulla

Biol. Reprod.

Oviductal secretions: will they be key factors for the future ARTs?

Mol. Hum. Reprod.

Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg

J. Biol. Chem.

Identification of CCR6, the specific receptor for a novel lymphocyte-directed CC chemokine LARC

J. Biol. Chem.

Induction of immune-related gene expression by seminal exosomes in the porcine endometrium

Biochem. Biophys. Res. Commun.

Induction of immune-related gene expression by seminal exosomes in the porcine endometrium

Biochem. Biophys. Res. Commun.

Greater numbers of human spermatozoa associate with endosalpingeal cells derived from the isthmus compared with those from the ampulla

Huamn Reprod.

Proteomics of post-translational modifications of mammalian spermatozoa

Cell Tissue Res.

Oviductal extracellular vesicles (oviductosomes, OVS) are conserved in humans: murine OVS play a pivotal role in sperm capacitation and fertility

Mol. Hum. Reprod.

Flow-cytometric evaluation of lectin binding moieties on porcine uterine epithelial cells

Reprod. Domest. Anim.

Sperm binding to porcine uterine epithelial cells might be lectin mediated

Reprod. Fertil. Dev.

Sulphated glycosaminoglycans (S-GAGs) and syndecans in the bovine oviduct

Anim. Reprod. Sci.

In vitro capacitation of bull spermatozoa by oviductal fluid and its components

Zygote

Effect of bovine oviduct epithelial cell apical plasma membranes on sperm function assessed by a novel flow cytometric approach

Biol. Reprod.

Localization of the chaperone proteins GRP78 and HSP60 on the luminal surface of bovine oviduct epithelial cells and their association with spermatozoa

Biol. Reprod.

Effects of bovine oviductal proteins on bull spermatozoal function

Theriogenology

Heparin and Ca2+-free medium can enhance release of bull sperm attached to oviductal epithelial cell monolayers

Theriogenology

Neutrophil extracellular traps kill bacteria

Science

Posttranslational modifications in spermatozoa and effects on male fertility and sperm viability

OMICS

Fertilization and early embryonic development in the porcine fallopian tube

Reprod. Domest. Anim.

Review
Sperm interactions with the female reproductive tract: A key for successful fertilization in mammals