Novel extracellular, extra-embryonic and intercellular γ-tubulin assemblies in mouse oocytes and preimplantation embryos

γ-tubulin is a core component of microtubule-organizing centers (MTOCs), which are traditionally known as intracellular. Here, we report previously unrecognized extracellular, intercellular, and extra-embryonic γ-tubulin assemblies in mouse oocytes and preimplantation embryos in three distinct categories: the γ-tubulin extracellular satellite (γ-TES), γ-tubulin intercellular bridge girdle (γ-IBG), and γ-tubulin nucleation center (γ-TNC). γ-TESs are punctate structures outside the plasma membrane of oocytes and pre-hatching embryos. γ-IBGs are transient, ring-like structures that, together with F-actin, encircle nascent intercellular bridges, suggesting a previously unrecognized role for γ-tubulin in early intercellular bridge formation. γ-TNCs are large, dynamic extracellular assemblies that emerge after fertilization and undergo stage-specific spatial and morphological reorganization during cleavage and blastocyst development. Both γ-TESs and γ-TNCs disappear after embryo hatching. Furthermore, γ-TNCs and γ-IBGs may represent large and ring-like aggregates of γ-TESs, respectively, suggesting that γ-TESs may serve as a local γ-tubulin reservoir for higher order formations. γ-IBGs and γ-TNCs also exhibit close spatial association with microtubules, which form a peri-embryonic web lining the edge of the embryo exterior from zygotes to morulae. Together, our findings reveal a non-canonical, extra-embryonic γ-tubulin organization system that may coordinate an embryonic skeleton architecture across blastomeres for critical embryo-wide developmental events such as polyspermy prevention, polarity establishment, morula and blastocyst formation, and embryo hatching.