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Oviduct and Pre-Implantation Embryo Growth and Development Intra-Uterine Migration and Spacing of Blastocysts Definitions • Trophectoderm: Cells forming the outer layer of a blastocyst which provide nutrients to blaostocyst and later participate in forming the chorion or outer layer of cells of the placenta. • Cytotrophoblast: Inner layer of trophectoderm to syncytiotrophoblast and external to the wall of the blastocyst; considered a trophoblastic stem cell as layer surrounding the blastocyst remains while daughter cells differentiate and proliferate to function in multiple roles as: 1) cytotrophoblast and syncytiotrophoblast. 1. Syncytotrophoblast 2. Cytotrophoblast 3. Endothelial Cells 4. Smooth Muscle Cells (tunica muscularis) 5. Spiral Artery 6. Endovascular cytotrophoblast Definitions (Continued) • Syncytiotrophoblast: multi-nucleated epithelial syncytrium covering highly vascular embryonic placental villi, which invade the wall of the uterus to establish nutrient circulation between the embryo and the mother. • Yolk Sac: Evagination of foregut of the embryo that provides nourishment and is site of development of circulatory and hematopoietic systems. • Allantois: evagination of hind gut of embryo for holding allantoic fluid and supports vasculature of chorioallantoic placenta. Definitions (Continued) • Chorion: membrane formed by extraembryonic mesoderm and ectoderm (sommatopleure) that surrounds the embryo/fetus and other placental membranes; chorionic villi emerge from the chorion to invade the endometrium; transfer of nutrients from maternal to fetal blood. • Amnion: membrane that immediately surrounds the embryo/fetus and fills with amniotic fluid to provide a protective environment for the developing embryo. PRE-IMPLANTATION EMBRYONIC DEVELOPMENT Morula To Blastocyst Transition Polarization Of Trophectoderm – Tight and Gap Junctions Outgrowth Of Trophectoderm Arg Leu Gwatkin, 1966; Martin and Sutherland, 2001 1- Zona Pellucida 2- Trophectoderm 3-Extra-embronic Endoderm 4-Blastocoel 5. Inner Cell Mass or Embryonic Disc Conceptus Development in Sheep D12 D13 7,889 UNDERGRADUATE D14 D15 2,859 GRADUATE D16 Cell Proliferation and Migration mRNA translation Cytoskeletal Changes in Trophectoderm Extra-Embryonic Coelom Sheep, Goat, Cow Pig and Horse Cat, Dog Primates, Rodents Uterine Microenvironment Histotroph Components • Enzymes • Growth Factors • Adhesion Proteins • Cytokines • Hormones • Transport proteins • NUTRIENTS G Johnson Secretions From Luminal (LE) And Glandular Epithelia (GE) Of Endometrium And Selective Transport of Nutrients and Proteins Down-Regulation of Progesterone Receptors in Uterine Epithelia by Progesterone: A Prerequsite for Implantation in Mammals • Decline in anti-adhesive Muc-1 • Increase in certain adhesive integrins • Change in patterns of epithelial gene expression THE OVIDUCT: TRANSPORT OF SPERM AND OVUM AND EMBRYO • EGG TRANSPORT IN THE OVIDUCT Different between species ► DISCONTINUOUS PROGRESSION (cow, ewe, monkey, baboon, human, guinea pig) Due to a prolonged stay at the Ampullary-Isthmic Junction Antiperistaltic contractions maintain egg for 2-3 days Stronger, peristaltic contractions then transport egg to isthmus and on into uterus Does not matter whether egg is fertilized or not ► SLOW, CONTINUOUS PROGRESSION (rabbit, pig, rodent) RABBIT Time (h) Event 0 Ovulation induced by hCG 18-24 All eggs found in ampulla and A-I junction 36 Eggs at A-I junction and distal isthmus 48 Eggs equally distributed between distal and proximal isthmus 60 2/3 eggs in proximal isthmus 63 90% eggs in proximal isthmus 72 All eggs in uterus ► FERTILIZED PROGRESSION (mare) Only fertilized eggs pass into uterus in mares (early pregnancy recognition) > Fertilization specific changes in ZP (mucopolysaccharide coat) > Embryo secretes prostaglandins (PG) E and F that are hypothesized to promote embryo migration through oviduct as well as in the uterus > Infusion of PGE2 into oviducts of pregnant mares hastened transport of oocytes and embryos into the uterus > Rat and hamster - fertilized eggs passage more rapidly and synchronously > Fertilized eggs may secrete motility regulatory factor(s) such as platelet activating factor (PAF) or prostaglandins > Cigarette smoke interferes with oocyte and embryo transport ► ROLE OF STEROIDS IN OVIDUCT MOTILITY Estradiol - accelerates egg passage if administered after ovulation, but causes a prolonged blockage of the eggs if administered at the time of ovulation > ovum transport is accelerated in superovulated animals > may involve membrane estrogen effects rather than nuclear Progesterone - shortens duration of tubal ovum transport if administered at ovulation Steroids affect smooth muscle contraction activity ROLE OF OVIDUCTAL SECRETIONS IN DEVELOPMENT OF FERTILIZED EGG > Physiological or biological role: OBLIGATORY vs FACILITORY ???? > Culture of zygote in various media leads to loss in viability or to a block in development - Block occurs at stage when embryonic genome becomes functional - Prepubertal oviduct can ensure activation of embryonic genome > Oviductal secretions, oviductal-specific proteins and oviductal epithelium enhance fertilization and embryonic development > Oviduct sustains and enhances fertilization and early cleavage-stage embryonic development Provides optimal environment in terms of temperature, pH, osmotic pressure, nutrients, oxygen tension and other factors Molecules found in the oviduct (Kane et al., 1997; Buhi et al., 2001) Amino acids, Glucose and fructose, Lipids, Albumin Oviductal proteins Protease inhibitors (TIMP-1, PAI-1) Retinol binding protein (RBP) Osteopontin (OPN) Large number of growth factors Transferrin Porcine oviduct secretory proteins (POSPs) (Buhi et al., 2001) -Estrogen enhances synthetic activity -Infundibulum and ampulla affected by estrogen, but not isthmus -Synthetic capacity: Infundibulum & ampulla > isthmus (2-3X) -Oviduct synthesized proteins are similar in each species -Major secretory product is a chitinase family member (cleaves chitin = N- acetylglucosamine polymer) - Binding of POSPs can be detected on the ZP and vitelline membrane Recent evidence in the pig indicates that pOSPs decrease the rate of polyspermy observed in IVF - Ligation of oviduct causes degeneration of blastocysts in rat and ewe - Tubal pregnancies only exists in humans INTRAUTERINE MIGRATION AND SPACING > Morulae differentiate into blastocysts 2-4 days postovulation and then enter uterus to become blastocyts (exception in domestic animals is the horse) > Myometrial contractility Increase in myometrial electrical or contractile activity Day 9 to 12 - sow 10 and 20 hours on Day 4 - rat > RAT Uterine motility before 5th day is involved in equidistribution of embryos Catecholamines Treatment of rats with α1 receptor blockers renders myometrium electrically quiescent and disorganizes embryo distribution Prostaglandins (PGs) Inhibitor of PG synthesis administered on Day 5 prevents regular distribution of implantation sites Estrogens Increase in myometrial electrical activity on Day 4 concomitant with increase in uterine E2 concentration Estrogen may directly stimulate myometrial contractility or increase myometrial sensitivity to catecholamines Administration of RU486 to rabbits or rats during passage of morulae into uterine horns causes accumulation at cervical extrimity and their expulsion > PIG In the pig, Day 10 to 12 embryos migrate through both uterine horns. Usually end up with 5 embryos in each horn. After migration, get spacing. Blastocyst migration and spacing Days 3-8 embryos in upper 1/3 of horn Days 9-10 mixing and migration of embryos Day 11 equal spacing Blastocyst produces estrogen which acts on uterine epithelium to release calcium Calcium may affect myometrium to cause contractions Blastocyst also produces PGF and PGE - may also act on myometrium Estrogen acts on uterine epithelium to cause release of histamine Histamine acts on myometrium EXPERIMENTAL EVIDENCE Pope et al., Biol Reprod 1982; 27:575-579; J Anim Sci 1982; 55:1169-1178. > Beads containing estrogen or cholesterol were inserted into uterine lumen on Day 7 On Day 12, beads impregnated with estrogen were found to migrate farther than those impregnated with cholesterol > Day 6 Px - subserosa of each uterine horn tip was injected with vehicle, 8 mg cromolyn sodium or 8 mg cromolyn sodium plus 1 mg histamine > Found that cromolyn sodium treatment alone restricted D10 embryos to tip of uterine horn, but Day 12 embryos overcame restriction. > Injection of histamine prevented actions of cromolyn sodium treatment Both E2 and histamine are involved in intrauterine migration of porcine embryos Uterine flushings from pregnant horns contained substance that, in part, mimicked the effects of embryo on in vitro myometrial contractility Flushings containing Day12 embryos overcame in vitro inhibitory effects of indomethacin on myometrial contractility > HORSE Blastocyst capsule has a mucin coat around it (MUC1) As long as capsule present, blastocyst is motile. Blastocysts migrate between horns (>12-15 times/day) Makes contact with uterine epithelium Embryo migration part of pregnancy recognition mechanism Stays mobile until Day 18 and then undergoes fixation (removal of MUC1) Horse Embryo DAY 12 • Edg7 (endothelial differentiation, lysophosphatidic acid G- protein-coupled receptor 7) – Also known as Lpa3 – Preference for unsaturated LPA • Knocked out Edg7 (Lpa3) • Grossly normal – litter size reduced by 50% – Pregnancy prolonged (1.5 days) ROLE OF CYTOKINES AND SECRETORY PROTEINS IN EARLY
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