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 |
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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 |
format | Article |
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[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.</description><identifier>ISSN: 0092-8674</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2023.10.003</identifier><identifier>PMID: 37922900</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>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</subject><ispartof>Cell, 2023-11, Vol.186 (24), p.5308-5327.e25</ispartof><rights>2023 The Authors</rights><rights>Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-9d98d4fdffe1ff5f846dcac0d857dc03491060608d4e48d6e8d5e09da6ca8783</citedby><cites>FETCH-LOGICAL-c400t-9d98d4fdffe1ff5f846dcac0d857dc03491060608d4e48d6e8d5e09da6ca8783</cites><orcidid>0000-0001-7726-1717</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.cell.2023.10.003$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37922900$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jentoft, Ida M.A.</creatorcontrib><creatorcontrib>Bäuerlein, Felix J.B.</creatorcontrib><creatorcontrib>Welp, Luisa M.</creatorcontrib><creatorcontrib>Cooper, Benjamin H.</creatorcontrib><creatorcontrib>Petrovic, Arsen</creatorcontrib><creatorcontrib>So, Chun</creatorcontrib><creatorcontrib>Penir, Sarah Mae</creatorcontrib><creatorcontrib>Politi, Antonio Z.</creatorcontrib><creatorcontrib>Horokhovskyi, Yehor</creatorcontrib><creatorcontrib>Takala, Iina</creatorcontrib><creatorcontrib>Eckel, Heike</creatorcontrib><creatorcontrib>Moltrecht, Rüdiger</creatorcontrib><creatorcontrib>Lénárt, Peter</creatorcontrib><creatorcontrib>Cavazza, Tommaso</creatorcontrib><creatorcontrib>Liepe, Juliane</creatorcontrib><creatorcontrib>Brose, Nils</creatorcontrib><creatorcontrib>Urlaub, Henning</creatorcontrib><creatorcontrib>Fernández-Busnadiego, Rubén</creatorcontrib><creatorcontrib>Schuh, Melina</creatorcontrib><title>Mammalian oocytes store proteins for the early embryo on cytoplasmic lattices</title><title>Cell</title><addtitle>Cell</addtitle><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.</description><subject>Animals</subject><subject>cryoelectron tomography</subject><subject>cytoplasmic lattices</subject><subject>Cytoskeleton</subject><subject>Embryo, Mammalian - metabolism</subject><subject>Embryonic Development</subject><subject>expansion microscopy</subject><subject>Female</subject><subject>female infertility</subject><subject>Mammals</subject><subject>maternal-to-zygotic transition</subject><subject>oocyte</subject><subject>Oocytes - metabolism</subject><subject>Pregnancy</subject><subject>protein storage</subject><subject>Proteins - metabolism</subject><subject>Ribosomes</subject><issn>0092-8674</issn><issn>1097-4172</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1LAzEQhoMotlb_gAfJ0cvW2exXFrxI8QtavPQe0mSCKbubmqRC_71ZWj3KHALD875MHkJuc5jnkNcP27nCrpszYEVazAGKMzLNoW2yMm_YOZkCtCzjdVNOyFUIWwDgVVVdkknRtIy1AFOyWsm-l52VA3VOHSIGGqLzSHfeRbRDoMZ5Gj-RovTdgWK_8QdH3UAT7HadDL1VtJMxWoXhmlwY2QW8Ob0zsn55Xi_esuXH6_viaZmpEiBmrW65Lo02BnNjKsPLWiupQPOq0QqKss2hTpMgLLmukesKodWyVpI3vJiR-2NtOvJrjyGK3obRhRzQ7YNgnNc1sIaNKDuiyrsQPBqx87aX_iByEKNFsRVjUowWx12ymEJ3p_79pkf9F_nVloDHI4Dpk98WvQjK4qBQW48qCu3sf_0_rHKEgg</recordid><startdate>20231122</startdate><enddate>20231122</enddate><creator>Jentoft, Ida M.A.</creator><creator>Bäuerlein, Felix J.B.</creator><creator>Welp, Luisa M.</creator><creator>Cooper, Benjamin H.</creator><creator>Petrovic, Arsen</creator><creator>So, Chun</creator><creator>Penir, Sarah Mae</creator><creator>Politi, Antonio Z.</creator><creator>Horokhovskyi, Yehor</creator><creator>Takala, Iina</creator><creator>Eckel, Heike</creator><creator>Moltrecht, Rüdiger</creator><creator>Lénárt, Peter</creator><creator>Cavazza, Tommaso</creator><creator>Liepe, Juliane</creator><creator>Brose, Nils</creator><creator>Urlaub, Henning</creator><creator>Fernández-Busnadiego, Rubén</creator><creator>Schuh, Melina</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7726-1717</orcidid></search><sort><creationdate>20231122</creationdate><title>Mammalian oocytes store proteins for the early embryo on cytoplasmic lattices</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c400t-9d98d4fdffe1ff5f846dcac0d857dc03491060608d4e48d6e8d5e09da6ca8783</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>cryoelectron tomography</topic><topic>cytoplasmic lattices</topic><topic>Cytoskeleton</topic><topic>Embryo, Mammalian - metabolism</topic><topic>Embryonic Development</topic><topic>expansion microscopy</topic><topic>Female</topic><topic>female infertility</topic><topic>Mammals</topic><topic>maternal-to-zygotic transition</topic><topic>oocyte</topic><topic>Oocytes - metabolism</topic><topic>Pregnancy</topic><topic>protein storage</topic><topic>Proteins - metabolism</topic><topic>Ribosomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jentoft, Ida M.A.</creatorcontrib><creatorcontrib>Bäuerlein, Felix J.B.</creatorcontrib><creatorcontrib>Welp, Luisa M.</creatorcontrib><creatorcontrib>Cooper, Benjamin H.</creatorcontrib><creatorcontrib>Petrovic, Arsen</creatorcontrib><creatorcontrib>So, Chun</creatorcontrib><creatorcontrib>Penir, Sarah Mae</creatorcontrib><creatorcontrib>Politi, Antonio Z.</creatorcontrib><creatorcontrib>Horokhovskyi, Yehor</creatorcontrib><creatorcontrib>Takala, Iina</creatorcontrib><creatorcontrib>Eckel, Heike</creatorcontrib><creatorcontrib>Moltrecht, Rüdiger</creatorcontrib><creatorcontrib>Lénárt, Peter</creatorcontrib><creatorcontrib>Cavazza, Tommaso</creatorcontrib><creatorcontrib>Liepe, Juliane</creatorcontrib><creatorcontrib>Brose, Nils</creatorcontrib><creatorcontrib>Urlaub, Henning</creatorcontrib><creatorcontrib>Fernández-Busnadiego, Rubén</creatorcontrib><creatorcontrib>Schuh, Melina</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jentoft, Ida M.A.</au><au>Bäuerlein, Felix J.B.</au><au>Welp, Luisa M.</au><au>Cooper, Benjamin H.</au><au>Petrovic, Arsen</au><au>So, Chun</au><au>Penir, Sarah Mae</au><au>Politi, Antonio Z.</au><au>Horokhovskyi, Yehor</au><au>Takala, Iina</au><au>Eckel, Heike</au><au>Moltrecht, Rüdiger</au><au>Lénárt, Peter</au><au>Cavazza, Tommaso</au><au>Liepe, Juliane</au><au>Brose, Nils</au><au>Urlaub, Henning</au><au>Fernández-Busnadiego, Rubén</au><au>Schuh, Melina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mammalian oocytes store proteins for the early embryo on cytoplasmic lattices</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2023-11-22</date><risdate>2023</risdate><volume>186</volume><issue>24</issue><spage>5308</spage><epage>5327.e25</epage><pages>5308-5327.e25</pages><issn>0092-8674</issn><eissn>1097-4172</eissn><abstract>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.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>37922900</pmid><doi>10.1016/j.cell.2023.10.003</doi><orcidid>https://orcid.org/0000-0001-7726-1717</orcidid><oa>free_for_read</oa></addata></record> |
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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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