The mammalian midbody and midbody remnant are assembly sites for RNA and localized translation.
Arc
ESCRT-III
EV
MB
MBR
MBsome
RBP
abscission
cytokinesis
intercellular bridge
large extracellular vesicle
midbody
midbody remnant
mitosis
translation
Journal
Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028
Informations de publication
Date de publication:
09 10 2023
09 10 2023
Historique:
received:
30
12
2022
revised:
20
06
2023
accepted:
17
07
2023
pmc-release:
09
10
2024
medline:
26
10
2023
pubmed:
9
8
2023
entrez:
8
8
2023
Statut:
ppublish
Résumé
Long ignored as a vestigial remnant of cytokinesis, the mammalian midbody (MB) is released post-abscission inside large extracellular vesicles called MB remnants (MBRs). Recent evidence suggests that MBRs can modulate cell proliferation and cell fate decisions. Here, we demonstrate that the MB matrix is the site of ribonucleoprotein assembly and is enriched in mRNAs that encode proteins involved in cell fate, oncogenesis, and pluripotency, which we are calling the MB granule. Both MBs and post-abscission MBRs are sites of spatiotemporally regulated translation, which is initiated when nascent daughter cells re-enter G1 and continues after extracellular release. MKLP1 and ARC are necessary for the localization and translation of RNA in the MB dark zone, whereas ESCRT-III is necessary to maintain translation levels in the MB. Our work reveals a unique translation event that occurs during abscission and within a large extracellular vesicle.
Identifiants
pubmed: 37552987
pii: S1534-5807(23)00357-X
doi: 10.1016/j.devcel.2023.07.009
pmc: PMC10592306
mid: NIHMS1920572
pii:
doi:
Substances chimiques
RNA
63231-63-0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1917-1932.e6Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM122893
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM139695
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM144352
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS115716
Pays : United States
Informations de copyright
Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of interests The authors declare no competing interests.
Références
J Cell Biol. 2020 Sep 7;219(9):
pubmed: 32673395
Cell Res. 2014 Feb;24(2):251-3
pubmed: 24126714
PLoS One. 2013 Oct 10;8(10):e77051
pubmed: 24130834
Cold Spring Harb Perspect Biol. 2012 Nov 01;4(11):
pubmed: 22960595
BMC Genomics. 2021 Jun 9;22(1):425
pubmed: 34103018
Science. 2004 Jul 2;305(5680):61-6
pubmed: 15166316
Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Nature. 2007 Mar 15;446(7133):329-32
pubmed: 17361185
Nature. 2020 May;581(7807):209-214
pubmed: 32405004
J Cell Biol. 2014 Oct 13;207(1):41-57
pubmed: 25287301
Methods Mol Biol. 2017;1524:189-201
pubmed: 27815904
Nature. 2017 Jun 8;546(7657):243-247
pubmed: 28562589
J Cell Biol. 2019 Dec 2;218(12):3903-3911
pubmed: 31690620
J Cell Biol. 2016 Aug 1;214(3):259-73
pubmed: 27458130
Nat Commun. 2016 Aug 03;7:12426
pubmed: 27484926
J Cell Biol. 2002 Mar 4;156(5):783-90
pubmed: 11877456
Nat Rev Mol Cell Biol. 2020 Jan;21(1):25-42
pubmed: 31705132
Tissue Cell. 1973;5(1):47-61
pubmed: 4693990
Nat Commun. 2020 Apr 22;11(1):1941
pubmed: 32321914
Neuron. 2018 May 16;98(4):754-766.e4
pubmed: 29772202
Am J Hum Genet. 2016 Aug 4;99(2):511-20
pubmed: 27453579
Trends Cell Biol. 2009 Nov;19(11):606-16
pubmed: 19733077
Mol Biol Cell. 2016 Oct 15;27(20):3052-3064
pubmed: 27559134
Nature. 2004 Aug 19;430(7002):908-13
pubmed: 15282614
Nucleic Acids Res. 2017 Jan 4;45(D1):D183-D189
pubmed: 27899595
Dev Cell. 2020 Oct 26;55(2):195-208.e5
pubmed: 32979313
FEBS Lett. 2010 Jun 18;584(12):2652-61
pubmed: 20371245
Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):413-8
pubmed: 22160674
Mol Biol Cell. 2004 Jul;15(7):3083-94
pubmed: 15075367
Elife. 2020 Aug 26;9:
pubmed: 32844748
Mol Biol Cell. 2002 Jun;13(6):1832-45
pubmed: 12058052
Curr Biol. 2011 Dec 6;21(23):R958-60
pubmed: 22153165
J Cell Sci. 2014 Sep 1;127(Pt 17):3840-51
pubmed: 25002399
Cell Mol Life Sci. 2013 Jun;70(12):2031-44
pubmed: 22968342
J Cell Sci. 2018 Aug 3;132(4):
pubmed: 29967034
Genes Dev. 2001 Aug 15;15(16):2083-93
pubmed: 11511540
Nat Commun. 2019 Jul 18;10(1):3181
pubmed: 31320617
Nat Cell Biol. 2013 Mar;15(3):325-34
pubmed: 23417121
Curr Biol. 2004 Sep 21;14(18):1685-93
pubmed: 15380073
Nat Rev Mol Cell Biol. 2017 May;18(5):285-298
pubmed: 28225081
Cytoskeleton (Hoboken). 2012 Nov;69(11):882-92
pubmed: 22927365
Dev Cell. 2014 Dec 8;31(5):525-38
pubmed: 25490264
Front Mol Biosci. 2021 Apr 08;8:658020
pubmed: 33898525
EMBO J. 2000 Nov 1;19(21):5711-9
pubmed: 11060022
Elife. 2016 Sep 07;5:
pubmed: 27602576
Exp Cell Res. 1979 Jul;121(2):395-9
pubmed: 446543
Wiley Interdiscip Rev RNA. 2011 Jan-Feb;2(1):42-57
pubmed: 21278925
Front Physiol. 2022 May 25;13:910759
pubmed: 35694405
Cell Cycle. 2014;13(21):3436-41
pubmed: 25485587
Dev Cell. 2014 Feb 10;28(3):253-67
pubmed: 24525186
J Cell Biol. 2020 Nov 2;219(11):
pubmed: 33053167
Science. 2009 Jun 26;324(5935):1729-32
pubmed: 19460965
PLoS One. 2011;6(5):e20489
pubmed: 21647379
Curr Biol. 2021 May 24;31(10):2203-2213.e5
pubmed: 33711249
Curr Biol. 2010 May 25;20(10):927-33
pubmed: 20451386
Nat Commun. 2011 Oct 18;2:503
pubmed: 22009035
Science. 2017 Sep 22;357(6357):
pubmed: 28935776
Science. 2020 Feb 7;367(6478):
pubmed: 32029601
Nat Commun. 2022 May 19;13(1):2781
pubmed: 35589693
Mol Cell Biol. 2001 Apr;21(8):2944-55
pubmed: 11283271
Front Cell Neurosci. 2015 Aug 28;9:325
pubmed: 26379497
Nat Rev Mol Cell Biol. 2021 Mar;22(3):165-182
pubmed: 32873929
J Cell Biol. 1982 Sep;94(3):654-61
pubmed: 7130277
Dev Cell. 2020 Oct 12;55(1):84-96
pubmed: 33049213
Science. 2011 Mar 25;331(6024):1616-20
pubmed: 21310966
J Cell Biol. 2017 Aug 7;216(8):2235-2237
pubmed: 28667121
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Mol Biol Cell. 2012 Mar;23(6):1024-34
pubmed: 22278743
Dev Cell. 2020 Oct 12;55(1):45-68
pubmed: 33049211
Semin Cell Dev Biol. 2010 Dec;21(9):909-16
pubmed: 20708087
Elife. 2015 Aug 25;4:
pubmed: 26305499
Curr Biol. 2022 Apr 25;32(8):R385-R397
pubmed: 35472432
J Cell Biol. 1988 Feb;106(2):431-9
pubmed: 2448315
Mol Biol Cell. 1998 Aug;9(8):2037-49
pubmed: 9693365
Science. 2015 Sep 18;349(6254):1334-8
pubmed: 26383951
Cell. 2008 Mar 7;132(5):832-45
pubmed: 18329369
J Cell Biol. 1977 Jun;73(3):672-84
pubmed: 873994
Commun Biol. 2021 Mar 25;4(1):400
pubmed: 33767328
Cell. 2018 Jan 11;172(1-2):275-288.e18
pubmed: 29328916
Cell. 2018 Nov 29;175(6):1492-1506.e19
pubmed: 30449617
J Cell Sci. 2010 Nov 1;123(Pt 21):3734-44
pubmed: 20940252
Nat Commun. 2019 Oct 4;10(1):4513
pubmed: 31586073
Trends Cell Biol. 2013 Mar;23(3):118-28
pubmed: 23245592
Mol Biol Cell. 2010 Oct 1;21(19):3293-303
pubmed: 20719964
Nature. 2018 Nov;563(7732):508-513
pubmed: 30464263
Curr Opin Cell Biol. 2018 Feb;50:27-34
pubmed: 29438904
Curr Stem Cell Rep. 2021 Dec;7(4):161-173
pubmed: 36303610
Science. 1998 Jan 23;279(5350):580-5
pubmed: 9438855
Curr Biol. 2019 Oct 21;29(20):3538-3548.e7
pubmed: 31607533
Curr Biol. 2018 Apr 23;28(8):R458-R470
pubmed: 29689230
Bioessays. 2013 May;35(5):472-81
pubmed: 23450621
Dev Cell. 2019 Sep 23;50(6):716-728.e6
pubmed: 31402283
Nat Cell Biol. 2011 Sep 11;13(10):1214-23
pubmed: 21909099
Nat Cell Biol. 2017 Jul;19(7):787-798
pubmed: 28604678
Cell. 2019 Sep 19;179(1):147-164.e20
pubmed: 31539493
J Neurooncol. 2012 Feb;106(3):519-29
pubmed: 21904957