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From Hatching Into Fetal Life in the P E in the P E in The R.C. Chebel. 2011. Use of Applied Reproductive Technologies (FTAI, FTET) to Improve the Reproductive Efficiency in Dairy Cattle. Acta Scientiae Veterinariae. 39(Suppl 1): s203 - s221. Acta Scientiae Veterinariae, 2011. 39(Suppl 1): s203 - s221. ISSN 1679-9216 (Online) From Hatching into Fetal Life in the Pig Poul Hyttel, Kristian M. Kamstrup & Sara Hyldig ABSTRACT Background: Potential adverse effects of assisted reproductive technologies may have long term consequences on embryonic and fetal development. However, the complex developmental phases occurring after hatching from the zona pellucida are less studied than those occurring before hatching. The aim of the present review is to introduce the major post-hatching developmental features bringing the embryo form the blastocyst into fetal life in the pig. Review: In the pre-hatching mouse blastocyst, the pluripotency of the inner cell mass (ICM) is sustained through expression of OCT4 and NANOG. In the pre-hatching porcine blastocyst, a different and yet unresolved mechanism is operating as OCT4 is expressed in both the ICM and trophectoderm, and NANOG is not expressed at all. Around the time of hatching, OCT4 becomes confined to the ICM. In parallel, the ICM is divided into a ventral cell layer, destined to form the hypoblast, and a dorsal cell mass, destined to form the epiblast. The hypoblast gradually develops into a complete inner lining along the epiblast and the trophectoderm. Upon hatching (around Day 7-8 of gestation), the trophectoderm covering the developing epiblast (Rauber´s layer) is lost and the embryonic disc is formed by development of a cavity in the epiblast, which subsequently “unfolds” resulting the establishment of the disc. In parallel, the epiblast initiates expression of NANOG in addition to OCT4. The blastocyst enlarges to a sphere of almost 1 cm around Day 10 of gestation. Subsequently, a dramatic elongation of the embryo occurs, and by Day 13 it has formed a thin approximately one meter long filamentous structure. This elongation is paralleled with the initiation of placentation along with which, the embryonic disc undergoes gastrulation. The latter process is preceded by a thickening of the posterior region of the epiblast, putatively developing as a consequence of an absence of inhibitory signals from a condensed portion of the hypoblast underlying the anterior epiblast. The thickened posterior epiblastN expresses the primitive streak marker BRACHYURY. Subsequently, the epiblast thickening extends in an anterior direction forming the primitive streak; also expressing BRACHYURY. Gastrulation is hereby initiated, and epiblast cells ingress through the primitive streak to form mesoderm and endoderm; the latter is inserted into the dorsal hypoblast whereas the mesoderm forms a more loosely woven mesenchyme between the epiblast and the endoderm. The anterior mesoderm, ingressing through the anterior end of the primitive streak, referred to as the node, forms the rod-like notochord interposed between the epiblast and the endoderm. During the subsequent neurulation, which is a process overlapping with gastrulation in time, the notochord induces the overlying epiblast to form neural ectoderm, which sequentially develops into the neural plate, neural groove, and neural tube, whereas the lateral epiblast develops into the surface ectoderm. In parallel with the development of the somatic germ layers, ectoderm, mesoderm, and endoderm, the primordial germ cells, the predecessors of the germ line, develop in the posterior epiblast and initiates a migration finally bringing them to the genital ridges of the developing embryo. In parallel, the ectoderm gives rise to the epidermis and neural tissue, the mesoderm develops into the cardiovascular system as well as the urogenital and musculoskeletal systems, whereas the endoderm forms the gastrointestinal system and related organs as the liver and pancreas. Conclusions: Porcine embryonic and fetal development is controlled by molecular mechanisms that to some degree differ from those operating in the mouse. It is of importance to uncover the molecular control of development in ungulates as it has great implications for assisted reproductive technologies as well as for biomedical model research. Keywords: Biomedical models, embryology, blastulation, gastrulation, neurulation, embryonic staging. CORRESPONDENCE: P. Hyttel [[email protected] – FAX: +45 353 32547]. Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, Groennegaardsvej 7, DK-1870 Frederiksberg C, Denmark. s203 R.C. Chebel. 2011. Use of Applied Reproductive Technologies (FTAI, FTET) to Improve the Reproductive Efficiency in Dairy Cattle. Acta Scientiae Veterinariae. 39(Suppl 1): s203 - s221. I. INTRODUCTION sarily a guarantee for further development into a fetus II.BLASTULATION: DEVELOPMENT OF TRO- and newborn. Hence, it is well-documented that in PHECTODERM, ICM, EPIBLAST, HYPOBLAST, vitro embryo culture may impose long-term effects, AND EMBRYONIC DISC which are revealed later during embryonic and fetal III. GASTRULATION: DEVELOPMENT OF MESO- development [40]. This phenomenon becomes even DERM, ENDODERM, AND ECTODERM more exaggerated when embryos are produced by 3.1 The primitive streak SCNT, which imposes an even higher risk of 3.2 Ingression of cells forming mesoderm and endoderm embryonic and fetal aberrations as well as neonatal IV. NEURULATION: DEVELOPMENT OF THE NEU- loss [9,35]. RAL ECTODERM AND NEURAL CREST In order to evaluate embryonic and fetal 4.1 Neural ectoderm development resulting from assisted reproductive 4.2 Neural crest technologies more properly, increasing focus should V. DEVELOPMENT OF THE PRIMORDIAL GERM be put on the normality of some of the complex post- CELLS (PGCS) hatching processes, as e.g. gastrulation, neurulation, VI. FURTHER DEVELOPMENT OF THE EMBRYO 6.1 The ectoderm and its early derivatives placentation and initial organogenesis, which are 6.2 The mesoderm and its early derivatives prerequisites for full term development. These pro- 6.3 Paraxial mesoderm cesses are the focus of the present review. Over the 6.4 Paraxial mesoderm past decade the pig has attracted increasing attention 6.5 Lateral plate mesoderm and body folding as a useful biomedical model, due to which the 6.6 Blood and blood vessel formation presented data will mainly be derived in this species. 6.7 The endoderm and its early derivatives Comparative notes will be made to cattle, whenever VII. PLACENTATION AND FORMATION OF EXTRA- the variation between these two species are pro- EMBRYONIC MEMBRANES AND CAVITIES nounced as e.g. at placentation. First, important deve- 7.1 Development of extra-embryonic membranes and lopmental processes of the general embryology inclu- cavities ding blastulation, gastrulation, neurulation, and deve- 7.2 Placentation lopment of the germ line will be presented, and, VIII. STAGING OF EMBRYONIC DEVELOPMENT second, a short summary of the special embryology, i.e. the development of the organ systems, will be IX. CONCLUSIONS given. I. INTRODUCTION II. BLASTULATION: DEVELOPMENT OF The wide-spread use of in vitro production TROPHECTODERM, ICM, EPIBLAST, HYPOBLAST, AND EMBRYONIC DISC of, in particular, bovine embryos in animal husbandry has paved the way for a detailed morphological and Blastulation (from the Greek term blastos molecular understanding of oocyte maturation, meaning sprout) is the process by which the embryo fertilization and initial embryonic development until develops into a fluid-filled structure in which the cells the time of hatching. Hence, studies on these life pro- have segregated into lines destined to produce the cesses have become facilitated by the easy embryo proper (the ICM and epiblast) and such accessibility of oocytes, zygotes, and embryos. developing into the extra-embryonic membranes (the Cloning by somatic cell nuclear transfer (SCNT) is trophectoderm and hypoblast). another technology, which over the past decade has In the pig, the blastocyst forms at around Day resulted in alternative in vitro production of 5 of gestation. The porcine embryo initiates com- considerable numbers of both bovine and porcine paction as early as the 8-16-cell stage, when the embryos adding to the accessibility of embryos for embryo assumes a spherical appearance with a research. Development of the embryo to the blastocyst smoother surface where the protrusions of the indi- stage includes several complex processes as e.g. the vidual blastomeres are no longer seen. The outer cells, activation of the embryonic genome (for review, see allocated to the trophectoderm, become connected Oestrup et al. [31]). It is also clear, however, that by tight junctions and desmosomes sealing the success in developing into a blastocyst is not neces- developing blastocyst cavity where the ICM forms s204 R.C. Chebel. 2011. Use of Applied Reproductive Technologies (FTAI, FTET) to Improve the Reproductive Efficiency in Dairy Cattle. Acta Scientiae Veterinariae. 39(Suppl 1): s203 - s221. as a cluster of lucent cells. Adjacent ICM cells com- that act upstream of CDX2 to mediate trophectoderm municate through scarce gap junctions [12]. The differentiation [26,28,47]. On the other hand, trophectoderm is divided into a polar portion, expression of the trophectoderm-associated transcri- covering the ICM, and a mural portion sealing the ption factors, CDX2, TEAD4, and ELF5, are blastocyst cavity. In advance of hatching, the ICM repressed in the ICM by the regulatory circuit of develops into a distinct
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