Mammalian oocytes store proteins for the early embryo on cytoplasmic lattices

Mammalian oocytes are filled with poorly understood structures called cytoplasmic lattices. First discovered in the 1960s and speculated to correspond to mammalian yolk, ribosomal arrays, or intermediate filaments, their function has remained enigmatic to date. Here, we show that cytoplasmic lattice...

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Veröffentlicht in:Cell 2023-11, Vol.186 (24), p.5308-5327.e25
Hauptverfasser: Jentoft, Ida M.A., Bäuerlein, Felix J.B., Welp, Luisa M., Cooper, Benjamin H., Petrovic, Arsen, So, Chun, Penir, Sarah Mae, Politi, Antonio Z., Horokhovskyi, Yehor, Takala, Iina, Eckel, Heike, Moltrecht, Rüdiger, Lénárt, Peter, Cavazza, Tommaso, Liepe, Juliane, Brose, Nils, Urlaub, Henning, Fernández-Busnadiego, Rubén, Schuh, Melina
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container_end_page 5327.e25
container_issue 24
container_start_page 5308
container_title Cell
container_volume 186
creator Jentoft, Ida M.A.
Bäuerlein, Felix J.B.
Welp, Luisa M.
Cooper, Benjamin H.
Petrovic, Arsen
So, Chun
Penir, Sarah Mae
Politi, Antonio Z.
Horokhovskyi, Yehor
Takala, Iina
Eckel, Heike
Moltrecht, Rüdiger
Lénárt, Peter
Cavazza, Tommaso
Liepe, Juliane
Brose, Nils
Urlaub, Henning
Fernández-Busnadiego, Rubén
Schuh, Melina
description Mammalian oocytes are filled with poorly understood structures called cytoplasmic lattices. First discovered in the 1960s and speculated to correspond to mammalian yolk, ribosomal arrays, or intermediate filaments, their function has remained enigmatic to date. Here, we show that cytoplasmic lattices are sites where oocytes store essential proteins for early embryonic development. Using super-resolution light microscopy and cryoelectron tomography, we show that cytoplasmic lattices are composed of filaments with a high surface area, which contain PADI6 and subcortical maternal complex proteins. The lattices associate with many proteins critical for embryonic development, including proteins that control epigenetic reprogramming of the preimplantation embryo. Loss of cytoplasmic lattices by knocking out PADI6 or the subcortical maternal complex prevents the accumulation of these proteins and results in early embryonic arrest. Our work suggests that cytoplasmic lattices enrich maternally provided proteins to prevent their premature degradation and cellular activity, thereby enabling early mammalian development. [Display omitted] •Oocytes store essential proteins for early embryogenesis on cytoplasmic lattices•Cytoplasmic lattices are composed of periodic filaments with high surface area•Many stored proteins are required for epigenetic reprogramming of the embryo•Study links infertility phenotypes in women with stored protein function Mammalian oocytes enrich proteins needed to sustain early embryonic development on cytoplasmic lattices. Loss of cytoplasmic lattices leads to reduced levels of maternally supplied proteins and embryogenesis failure.
doi_str_mv 10.1016/j.cell.2023.10.003
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First discovered in the 1960s and speculated to correspond to mammalian yolk, ribosomal arrays, or intermediate filaments, their function has remained enigmatic to date. Here, we show that cytoplasmic lattices are sites where oocytes store essential proteins for early embryonic development. Using super-resolution light microscopy and cryoelectron tomography, we show that cytoplasmic lattices are composed of filaments with a high surface area, which contain PADI6 and subcortical maternal complex proteins. The lattices associate with many proteins critical for embryonic development, including proteins that control epigenetic reprogramming of the preimplantation embryo. Loss of cytoplasmic lattices by knocking out PADI6 or the subcortical maternal complex prevents the accumulation of these proteins and results in early embryonic arrest. Our work suggests that cytoplasmic lattices enrich maternally provided proteins to prevent their premature degradation and cellular activity, thereby enabling early mammalian development. [Display omitted] •Oocytes store essential proteins for early embryogenesis on cytoplasmic lattices•Cytoplasmic lattices are composed of periodic filaments with high surface area•Many stored proteins are required for epigenetic reprogramming of the embryo•Study links infertility phenotypes in women with stored protein function Mammalian oocytes enrich proteins needed to sustain early embryonic development on cytoplasmic lattices. 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subjects Animals
cryoelectron tomography
cytoplasmic lattices
Cytoskeleton
Embryo, Mammalian - metabolism
Embryonic Development
expansion microscopy
Female
female infertility
Mammals
maternal-to-zygotic transition
oocyte
Oocytes - metabolism
Pregnancy
protein storage
Proteins - metabolism
Ribosomes
title Mammalian oocytes store proteins for the early embryo on cytoplasmic lattices
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