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Physiology and Regulation of Oviductal Secretions

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Physiology and Regulation of Oviductal Secretions International Journal of Molecular Sciences Review Composing the Early Embryonic Microenvironment: Physiology and Regulation of Oviductal Secretions Marie Saint-Dizier 1,2,* , Jennifer Schoen 3, Shuai Chen 3, Charles Banliat 2,4 and Pascal Mermillod 2 1 Faculty of Sciences and Techniques, Department Agrosciences, University of Tours, 37200 Tours, France 2 Institut National de la Recherche Agronomique (INRA), UMR85 Physiologie de la Reproduction et des Comportements, CNRS 7247, University of Tours, IFCE, 37380 Nouzilly, France; [email protected] (C.B.); [email protected] (P.M.) 3 Leibniz Institute for Farm Animal Biology, FBN Dummerstorf, 18196 Dummerstorf, Germany; [email protected] (J.S.); [email protected] (S.C.) 4 Union Evolution, Rue Eric Tabarly, 35538 Noyal-Sur-Vilaine, France * Correspondence: [email protected]; Tel.: +33-247-427-508 Received: 18 November 2019; Accepted: 25 December 2019; Published: 28 December 2019 Abstract: The oviductal fluid is the first environment experienced by mammalian embryos at the very beginning of life. However, it has long been believed that the oviductal environment was not essential for proper embryonic development. Successful establishment of in vitro embryo production techniques (which completely bypass the oviduct) have reinforced this idea. Yet, it became evident that in vitro produced embryos differ markedly from their in vivo counterparts, and these differences are associated with lower pregnancy outcomes and more health issues after birth. Nowadays, researchers consider the oviduct as the most suitable microenvironment for early embryonic development and a substantial effort is made to understand its dynamic, species-specific functions. In this review, we touch on the origin and molecular components of the oviductal fluid in mammals, where recent progress has been made thanks to the wider use of mass spectrometry techniques. Some of the factors and processes known to regulate oviductal secretions, including the embryo itself, as well as ovulation, insemination, endogenous and exogenous hormones, and metabolic and heat stress, are summarized. Special emphasis is laid on farm animals because, owing to the availability of sample material and the economic importance of fertility in livestock husbandry, a large part of the work on this topic has been carried out in domestic animals used for dairy and/or meat production. Keywords: oviduct; fallopian tube; tubal fluid; female genital tract; cattle; pig; embryo development 1. Introduction The oviduct has long been considered as a pipeline for the meeting of gametes at ovulation and transport of the embryo to the uterus. From the late 1970s, it became possible to bypass the oviduct and produce mammalian embryos in vitro, leading to the idea that only minimal components of the oviduct were necessary to support embryo development. However, since then, a number of studies showed that the morphology, gene expression, and lipid and protein composition of the in vitro produced embryos differ markedly from their in vivo counterparts, and that these differences are associated with lower pregnancy outcomes and more health issues after birth [1–4]. Forty years after the first in vitro fertilization (IVF) success and in parallel with limited progress in the field, researchers consider the oviduct as the most suitable microenvironment for early embryo development and substantial effort has been made to understand its dynamic species-specific functions. The oviduct is indeed the first interface between the female genital tract and the conceptus, mediating an early Int. J. Mol. Sci. 2020, 21, 223; doi:10.3390/ijms21010223 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 21 Int. J. Mol. Sci. 2020, 21, 223 2 of 21 mediating an early embryo–maternal dialog through cell contacts, secreted molecules, and extracellular vesicles (EVs) [5–7]. However, studying the physiology of the oviduct and its secretions embryo–maternal dialog through cell contacts, secreted molecules, and extracellular vesicles (EVs) [5–7]. to better understand the needs of the embryo is challenging. First, the oviducts are small intra- However, studying the physiology of the oviduct and its secretions to better understand the needs abdominal organs, not accessible without surgery or animal slaughter and filled with only microliters of the embryo is challenging. First, the oviducts are small intra-abdominal organs, not accessible of fluid.without Moreover, surgery ormany animal steps slaughter in a andrelatively filled with short only period microliters of time of fluid. take Moreover, place before many stepsembryo developmentin a relatively in the short oviduct, period that of timeis, sperm take place storage, before sperm embryo transport development and capacitation, in the oviduct, uptake that is, and transportsperm of storage, the cumulus–oocyte sperm transport comp and capacitation,lex (COC), uptake and finally and transport fertilization, of the cumulus–oocyte with each step complex being able to modify(COC), the and embryonic finally fertilization, microenvironment with each step (Figure being able1). Beside to modify these the internal embryonic factors, microenvironment various factors outside(Figure the 1oviduct). Beside are these susceptibl internal factors,e to regulate various the factors oviduct outside microenvironment, the oviduct are susceptible including to regulate metabolic and environmentalthe oviduct microenvironment, stress. The aim including of this metabolic review and is environmentalto provide recent stress. Thedata aim on of the this molecular review compoundsis to provide of the recent tubal data fluid on theand molecular summarize compounds the factors of the that tubal can fluid dynamically and summarize change the factorsthe early embryonicthat can microenvironment. dynamically change Because the early of embryonic ethical constraints; microenvironment. availability Because of sample of ethical material; constraints; and last availability of sample material; and last but not least, the economic importance of fertility in livestock but not least, the economic importance of fertility in livestock husbandry, a large part of the work on husbandry, a large part of the work on this topic has involved farm animals, and this review will this topic has involved farm animals, and this review will largely focus on these species. largely focus on these species. Figure 1. Schematic representation of some factors and processes responsible for changes in the Figureoviductal 1. Schematic microenvironment representation before of andsome during factors embryonic and processes development. responsible Prior to ovulationfor changes sperm in the oviductalinteract microenvironment with the epithelial liningbefore of and the oviduct. during Afterembryonic ovulation, development. the ovulated oocytePrior withto ovulation surrounding sperm interactcumulus with cellsthe asepithelial well as the lining developing of the embryo oviduc influencet. After oviductal ovulation, functions the both ovulated mechanically oocyte and with surroundingvia para- /cumulusjuxtacrine cells signaling. as well Throughout as the developing the cycle, ovarian embryo sex steroidsinfluence produced oviductal by thefunctions follicle(s) both mechanicallyand corpora and lutea via para-/juxtacrine modulate oviductal signaling. secretions. Throughout the cycle, ovarian sex steroids produced by2. Originthe follicle(s) and Renewal and corpora of the lutea Tubal modulate Fluid oviductal secretions. 2. Origin Theand oviductalRenewal fluidof the (OF) Tubal is predominantly Fluid composed by the oviduct epithelium and consists of components that are either passively or actively transported over the epithelial barrier from the Thecirculating oviductal blood fluid or the(OF) interstitial is predominantly tissue, or composed de novo secreted by the byoviduct the oviduct epithelium epithelial and cells consists [8]. of componentsThe oviduct that lumen are either is lined passively by a simple, or columnar-shaped actively transported epithelium over containing the epithelial both non-ciliated barrier from and the circulatingciliated blood cells (Figureor the 2interstitial). Although tissue, non-ciliated or de cellsnovo are secreted also called by the ‘secretory oviduct non-ciliated epithelial cells’,cells it[8]. is The oviductmost lumen likely is that lined both by non-ciliated a simple, and columnar-shape ciliated cells participated epithelium in oviductal containing secretions both (Figure non-ciliated3). and ciliated cells (Figure 2). Although non-ciliated cells are also called ‘secretory non-ciliated cells’, it is most likely that both non-ciliated and ciliated cells participate in oviductal secretions (Figure 3). Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 3 of 21 Int. J. Mol. Sci. 2020, 21, 223 3 of 21 Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 3 of 21 Figure 2. The oviduct lumen is lined by a simple, columnar-shaped epithelium containing non-ciliated Figure 2. The oviduct lumen is lined by a simple, columnar-shaped epithelium containing non-ciliated andFigure ciliated 2. The cells. oviduct Immunolocalization lumen is lined by a simple,of acetylated columnar-shaped tubulin epithelium(A,B; green) containing in porcine non-ciliated oviduct and ciliated cells. Immunolocalization of acetylated tubulin (A,B; green) in porcine oviduct epithelium epitheliumand ciliated visualizes cells. Immunolocalizationmotile cilia bordering of theacetylated lumen. Epithelialtubulin
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