The oocyte/zygote of drosophila and nematode as a model of evolutionary conservative processes in the early development of mammals and humans

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Abstract

Understanding the molecular mechanisms of oocyte maturation, as well as early embryonic development, is of fundamental importance not only for embryology, but also for medical biology. However, the difficulties of experimental studies of this kind of problems in mammals, and especially in humans, are obvious. It is also well known that many key processes and mechanisms of oogenesis — early embryogenesis are highly evolutionarily conserved. They can be traced from the level of the most studied model invertebrates, such as Drosophila D. melanogaster and roundworm C. elegans, to mammals and humans. In this review, using these model invertebrates as an example, in comparison with model vertebrates, we will discuss the conservatism of such key processes and mechanisms as: (1) Transport/localization of mRNA by molecular motors; (2) Calcium wave; (3) Transport/localization of molecules by cytoplasmic streaming; (4) Segregation of determinant molecules by PAR protein networks; (5) Segregation of determinant molecules by actin filaments and myosins. The most general problem in this area is how cytoskeletal structures and protein networks are organized and reorganized, and how they interact with calcium waves, cytoplasmic streaming, and active transport by molecular motors. It is important that these conserved processes interact with each other, and the modes and mechanisms of their interaction also tend to be conservative. Thus, the transport of developmental determinants by motors along the cytoskeleton is interconnected with virtually all other processes. It is also significant that these processes and mechanisms also tend to form conservative scenarios. Thus, the prototypical scenario calcium wave → reorganization of actin-myosin cytoskeleton → generation of cytoplasmic flows can be traced back to mammals and humans, and is easier to study in detail in models. Finally, many of the conserved components under consideration turn out to be involved in pathological processes, including oncology. Thus, genes and the factors of the PAR network encoded by them, key to the mechanisms of cellular polarization, are characterized as oncogenes/oncofactors for a number of model objects. Analysis of large-scale studies of the processes and mechanisms of early development of model organisms raises a number of general evolutionary questions, discussed in the conclusion of this review.

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About the authors

A. V. Spirov

Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Author for correspondence.
Email: alexander.spirov@gmail.com
Russian Federation, St. Petersburg

E. M. Myasnikova

Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences

Email: alexander.spirov@gmail.com
Russian Federation, St. Petersburg

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2. Fig. 1. Microtubule (MT) networks involved in active mRNA transport in oogenesis of model objects. (a–d) — organization and reorganization of MT networks in Drosophila oogenesis: (a) — in early Drosophila oogenesis, oriented MTs connect the oocyte with nurse cells through ring canals; (b) — dense and weakly oriented MT network in the oocyte at the middle stage of development; (b’) — localization of three major mRNA determinants (gurken, oskar, and bicoid) in the middle oocyte; (c) — oriented MT bundles in the mature oocyte, running under the cortex. (d–e) — mechanisms of localization of mRNA determinants in the cortex of the animal/vegetative pole of vertebrates by active transport motors along oriented MTs (the inset schematically shows a diagram of a kinesin molecule with an adapter and cargo): (d) — transport and localization of Vg1 mRNA in oocytes of the amphibian xenopus X. leavis; (e) — transport and localization of cyclin B1 mRNA in oocytes of the zebra fish D. rerio. Nu — nucleus, MTOC — MT organization centers.

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3. Fig. 2. Schematic diagram of the establishment of the core bicoid mRNA transport system in the earliest embryo (and unfertilized egg). As an inspiring example, the authors [37] took known ideas about the organization and behavior of the sperm aster at this stage of early embryogenesis (a). (b–c) are the results of 3D agent-based modeling: the cargo is concentrated in the core cytoplasm of the embryo’s head [37]. Arrows in (b) show the general direction of movement of the “cargo” along the MT. The image is an “optical” section of the central part of the embryo’s head end. The MT is colored green, the cargo is bright blue.

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4. Fig. 3. Dynamics of bcd mRNA (in complex with the Stau factor) for the early Drosophila embryo - from its release in the apical cortex (a) as a result of fertilization to the early 14th cycle stage (b). See text for details.

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5. Fig. 4. Organization and role of cytoplasmic flows in oocytes of several model objects of developmental biology: (a) — schematic picture of fast cytoplasmic flows in Drosophila oocytes during late oogenesis; (b) — cytoplasmic flows in the syncytial gonad of Caenorhabditis elegans move materials into the growing oocyte; (c) — cytoplasmic flows in a mouse oocyte before fertilization. In mouse oocytes, actin flows induce cytoplasmic flows, so that both these processes induce spindle migration (shown schematically). (d) — cytoplasmic flows in mouse oocytes after fertilization are characterized by two stages. Nu — nucleus; currents are shown by arrows.

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6. Fig. 5. Polarity in oocytes and embryos of the model objects roundworm C. elegans, Drosophila and mouse, determined by the activity of PAR networks [3]. Polarized distribution of PAR proteins (and accompanying factors) in the roundworm zygote (a), in the oocyte, neuroblast and epithelial cells of Drosophila (b) and in the oocyte and 16-cell embryo of mouse (c). Аnt — anterior pole; Pst — posterior pole, A — animal pole; V — vegetal pole. The names of the PAR network factors distributed in a polarized manner are given under each scheme.

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7. Fig. 6. Formation and role of actomyosin structures in the cortex of the early Drosophila embryo, the roundworm C. elegans, and the dividing stem cell (neuroblast). (a) — formation of contractile structures based on bipolar myosin II and actin filaments in the cortex of the early Drosophila embryo by the 6th nuclear cycle, so that the actomysin cortical network forms a contractile “coupling” approximately in the middle of the embryo. Contractions of this structure are believed [21] to generate cytoplasmic currents in the core part of the embryo directed toward the poles (shown by arrows). (b) — coordinated processes of local expansion of the cytoplasmic membrane (arrowheads) and displacement (currents) of myosin (curved arrows) in the processes of neuroblast ACD. As a result of such highly coordinated processes, myosin is concentrated in the area of ​​the future cleavage furrow, where its contractile activity ensures cytokinesis. (c) Segregation of PAR complexes (anterior and posterior), synchronized with myosin redistribution, and formation of the actomyosin contractile ring in the first cleavage division of the roundworm zygote. See text.

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