What is the relationship between the metabolism of preimplantation embryos and their developmental competence?

• Published in: Molecular reproduction and development Vol. 43; no. 1; pp. 105 - 133
• Main Authors: Barnett, D.K. (University of Wisconsin-Madison, Madison, WI.), Bavister, B.D
• Format: Journal Article
• Language: English
• Published: Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.01.1996; Wiley-Liss
• Subjects: Amino Acids; Amino Acids - analysis; analysis; Animals; BIOCHEMICAL PATHWAYS; Biological and medical sciences; Blastocyst; Blastocyst - metabolism; Blastocyst - physiology; CONSOMMATION D'OXYGENE; CONSUMO DE OXIGENO; CULTURE MEDIA; DESARROLLO EMBRIONARIO; DEVELOPPEMENT EMBRYONNAIRE; DURACION; DURATION; DUREE; Early stages. Segmentation. Gastrulation. Neurulation; embryo (animal); embryogenesis; Embryology: invertebrates and vertebrates. Teratology; Embryonic and Fetal Development; EMBRYONIC DEVELOPMENT; ENERGY METABOLISM; ENERGY PRODUCTION; Fatty Acids; Fatty Acids - metabolism; Female; Fundamental and applied biological sciences. Psychology; GESTACION; GESTATION; Glucose; Glucose - metabolism; Glycolysis; Humans; in vitro development; LITERATURE REVIEWS; Luminescent Measurements; mammalian embryo; Mammals; MEDIO DE CULTIVO; metabolism; METABOLISME ENERGETIQUE; METABOLISMO ENERGETICO; Microscopy, Fluorescence; MILIEU DE CULTURE; Mitochondria; Mitochondria - metabolism; Models, Biological; Organ Culture Techniques; OXYGEN CONSUMPTION; physiology; PREGNANCY; preimplantation; PREIMPLANTATION PERIOD; SUBSTRATES; VIA BIOQUIMICA DEL METABOLISMO; VOIE BIOCHIMIQUE DU METABOLISME; Embryonic development; Vertebrata; Mammalia; Embryo culture; Blastocyte; Review; Metabolism; In vitro
• ISSN: 1040-452X; 1098-2795
• DOI: 10.1002/(SICI)1098-2795(199601)43:1<105::AID-MRD13>3.0.CO;2-4

Although mammalian embryo development may be considered strictly to begin with the formation of an oocyte, and progresses through implantation, organogenesis, and fetal growth, it is beyond the scope of this review to cover such a vast topic. Accordingly, this review is limited to the preimplantation period, i.e., from the one-cell embryo to the blastocyst. The preimplantation embryo at its simplest level is a cell or a group or cells programmed to cleave repeatedly while progressively making the transition from maternal to autonomous genomic control. The theme of this review is the relationship between metabolism of the preimplantation embryo and its ability to undergo normal development in vitro ("normal" is defined as being competent to produce viable offspring after embryo transfer). Much has been published on the subject of embryo metabolism, yet there appear to be some underlying assumptions that could be inaccurate or even misleading. Metabolic data on embryos nearly always relate to substrate uptake or catabolism, but have rarely been placed in context with energy production (ATP content and turnover). Moreover, data are not well linked to the embryos' ability to complete developmentally important events such as cleavage and blastocoel cavity formation, or to viability. Thus, much of the present information on embryo metabolism is not helpful for understanding how embryos develop or what distinguishes a developmentally competent embryo. An apparent dichotomy between results from metabolic experiments and data from embryo culture studies reflects the lack of integration of these two approaches. For example, glucose is not metabolized to any great extent during the early cleavage stages of embryo development, so we might expect it to have little effect on development of embryos during this period. But glucose is moderately or even severely inhibitory to embryo development in vitro in most species studied except for some strains of inbred mice. An underlying problem is that, with very few exceptions, embryo development has been studied under one broad set of conditions, i.e., "culture" conditions, while metabolism has been examined under different types of "incubation" conditions that are suboptimal for or even inimical to embryo development. The importance of the relationship between culture media composition and embryo development is well recognized, but not well characterized. In general, it is insufficiently recognized that commonly used incubation conditions may actually alter embryo metabolism. If embryos are incubated in media that are suboptimal or detrimental, what is the functional relevance of metabolic data obtained under such conditions? Obviously, metabolism of embryos should be examined under culture conditions capable of supporting normal development, and the ability of embryos to continue development following exposure to (e.g.) radiolabeling conditions should be established. However, rarely have either of these approaches been adopted. Much of the available information may reflect, like a distorting mirror, metabolism imposed on the embryo by a constraining incubation environment, rather than represent processes functionally important for embryo development. Our concepts of substrate utilization by preimplantation embryos may need to be thoroughly re-evaluated.