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The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte

Nature Reviews Molecular Cell Biology volume 14, pages 141–152 (2013)Cite this article

Subjects

Key Points

  • The growth and the onset of meiotic maturation of the mammalian oocyte are controlled by bidirectional interactions between the oocyte and the surrounding somatic cells.

  • Junctional complexes and transzonal projections (TZPs) form the structural basis for the passage of signalling molecules and metabolic substrates that support oocyte growth.

  • The meiotic spindle forms through self-organization of microtubules and motor proteins in response to a RAN GTPase-mediated chromatin signal in the absence of centriole-containing centrosomes.

  • Meiotic chromatin provides a signal for the establishment of oocyte cortical polarity, which required for asymmetric meiotic cell divisions and leads to polar body extrusion.

  • Asymmetric positioning of the meiosis I spindle is established through actin-based forces that are regulated by actin nucleating factors, including a formin-family protein and the actin-related protein 2/3 (ARP2/3) complex.

  • Actin-driven cytoplasmic streaming contributes to the establishment and maintenance of oocyte polarity, and the parameters of post-fertilization streaming may be prognostic of the developmental potential of the embryo.

Abstract

Mammalian oocytes go through a long and complex developmental process while acquiring the competencies that are required for fertilization and embryogenesis. Recent advances in molecular genetics and quantitative live imaging reveal new insights into the molecular basis of the communication between the oocyte and ovarian somatic cells as well as the dynamic cytoskeleton-based events that drive each step along the pathway to maturity. Whereas self-organization of microtubules and motor proteins direct meiotic spindle assembly for achieving genome reduction, actin filaments are instrumental for spindle positioning and the establishment of oocyte polarity needed for extrusion of polar bodies. Meiotic chromatin provides key instructive signals while being 'chauffeured' by both cytoskeletal systems.

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Figure 1: Follicle development and interaction of the oocyte with somatic cells.
Figure 2: Maturation of a mammalian oocyte.
Figure 3: Features of the assembling meiotic spindle.
Figure 4: RAN mediates a signal from chromatin to induce cortical actomyosin assembly.
Figure 5: Possible mechanisms of force generation in spindle and chromosome movement.
Figure 6: Patterns of cytoplasmic streaming in the oocyte of several animal models.

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Acknowledgements

This work is supported in part by a grant from the US National Institutes of Health (NIH) (grant P01 GM 066311) (to R.L.) and an ESHE fund (to D.F.A.). The authors apologize to the researchers whose work could not be cited owing to space limitations, especially those who have developed many transgenic lines that have revealed so much about mouse oocyte biology.

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Authors and Affiliations

  1. Stowers Institute for Medical Research, 1000 East 50th Street, Kansas City, 64110, Missouri, USA

    Rong Li

  2. Department of Molecular and Integrative Physiology, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, 66160, Kansas, USA

    Rong Li & David F. Albertini

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  1. Rong Li
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Glossary

Polar body

The daughter cell which is much smaller than the oocyte that results from each of the two meiotic cell divisions. The first polar body mostly degenerates within hours of formation, whereas the second polar body persists intact through the early cleavage stages of embryonic development.

Gap junctions

Intercellular channel structures formed by connexin proteins that connect neighbouring cells to allow passage of nutrients, ions and signalling molecules.

Adherens junctions

Protein complexes that contain cadherin and catenin proteins. They are formed between neighbouring cells in the tissue and serve not only to maintain cell–cell adhesion but also to regulate intracellular signalling and cytoskeletal organization.

Maternal effect

Refers to when the phenotype of an organism reflects the genotype of the mother (rather than its own genotype). This is often due to the mother supplying gene products (mRNA and/or proteins) to the embryo.

Germinal vesicle

The large nucleus of the primary oocyte before meiosis is completed.

Polyspermy

Referring to one egg being fertilized by multiple sperms.

Microtubule-organizing centres

(MTOCs). Major sites of microtubule nucleation and anchoring. MTOCs in mammalian meiotic spindles lack centrioles and are inherited by the embryos until embryos are able to assemble centriole-containing centrosomes.

Bivalents

Paired homologous chromosomes in meiosis I.

Reductional chromosome segregation

During meiosis I, pairs of homologous chromosomes segregate to opposite sides of the cell division plane, resulting in daughter cells with half of the chromosome number of the immature oocyte or somatic cells.

Equational chromosome segregation

During meiosis II, sister chromatids separate and segregate to the two daughter cells, thus maintaining the same chromosome number as the post-meiosis I oocyte.

Centrosomes

Organelles that function as the main microtubule organizing centres (MTOCs) in animal cells. They comprise two orthogonally arranged centrioles surrounded by an amorphous protein mass termed the pericentriolar material (PCM). Centrosomes nucleate the mitotic spindle and regulate cell cycle progression.

Parthenogenetic embryos

Embryos obtained by asexual reproduction, whereby embryo growth and development occur without fertilization.

Partitioning defective 3

(PAR3). A member of the conserved family of PAR proteins, which polarize cells during animal development.

Actin-related protein 2/3

(ARP2/3). A highly conserved seven-subunit protein complex that contains two actin-related proteins, ARP2 and ARP3, and nucleates an actin filament at a ∼70° angle from the side of an existing actin filament.

Formin

Formins are an evolutionarily conserved family of actin nucleators. Their nucleation activity is accomplished by a dimer of the formin homology 2 (FH2) domain that then tracks along the elongating actin barbed end.

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Li, R., Albertini, D. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol 14, 141–152 (2013). https://doi.org/10.1038/nrm3531

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