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Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin

Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin
Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin
Aging is associated with the accumulation of several types of damage: in particular, damage to the proteome. Recent work points to a conserved replicative rejuvenation mechanism that works by preventing the inheritance of damaged and misfolded proteins by specific cells during division. Asymmetric inheritance of misfolded and aggregated proteins has been shown in bacteria and yeast, but relatively little evidence exists for a similar mechanism in mammalian cells. Here, we demonstrate, using long-term 4D imaging, that the vimentin intermediate filament establishes mitotic polarity in mammalian cell lines and mediates the asymmetric partitioning of damaged proteins. We show that mammalian JUNQ inclusion bodies containing soluble misfolded proteins are inherited asymmetrically, similarly to JUNQ quality-control inclusions observed in yeast. Mammalian IPOD-like inclusion bodies, meanwhile, are not always inherited by the same cell as the JUNQ. Our study suggests that the mammalian cytoskeleton and intermediate filaments provide the physical scaffold for asymmetric inheritance of dynamic quality-control JUNQ inclusions. Mammalian IPOD inclusions containing amyloidogenic proteins are not partitioned as effectively during mitosis as their counterparts in yeast. These findings provide a valuable mechanistic basis for studying the process of asymmetric inheritance in mammalian cells, including cells potentially undergoing polar divisions, such as differentiating stem cells and cancer cells.
Actins/metabolism, Aging/metabolism, Animals, CHO Cells, Cell Compartmentation/physiology, Cricetulus, HEK293 Cells, HeLa Cells, Humans, Inclusion Bodies/metabolism, Intermediate Filaments/metabolism, Mammals, Mice, Microscopy, Confocal/methods, Mitosis/physiology, Neuroblastoma, Proteasome Endopeptidase Complex/metabolism, Protein Folding, Saccharomyces cerevisiae, Spindle Apparatus/metabolism, Stress, Physiological/physiology, Vimentin/chemistry
0027-8424
8049-54
Ogrodnik, Mikołaj
c34798e9-a848-48f4-8d62-b1fd4d2053e8
Salmonowicz, Hanna
593929dc-86c9-46b1-8738-60be78ff9c66
Brown, Rachel
6a00909e-6ed5-4b82-8532-71909045784b
Turkowska, Joanna
17ac0df5-1c4d-4ed3-a4f5-fa2b9a604cb1
Średniawa, Władysław
c04f36f6-837c-42d4-a96f-c8dff3195c05
Pattabiraman, Sundararaghavan
a9f5aac6-6388-4b65-ba29-33aa47aad5a4
Amen, Triana
8dea95c1-8a56-4396-835a-bb7ef5d30ffb
Abraham, Ayelet-chen
9d7bdc49-a883-463d-acce-8635fa88e8b1
Eichler, Noam
ddf58cbc-1616-4704-80fc-65484d21986c
Lyakhovetsky, Roman
dd9f00c5-a583-4a79-a61a-b3088fa6e380
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
et al.
Ogrodnik, Mikołaj
c34798e9-a848-48f4-8d62-b1fd4d2053e8
Salmonowicz, Hanna
593929dc-86c9-46b1-8738-60be78ff9c66
Brown, Rachel
6a00909e-6ed5-4b82-8532-71909045784b
Turkowska, Joanna
17ac0df5-1c4d-4ed3-a4f5-fa2b9a604cb1
Średniawa, Władysław
c04f36f6-837c-42d4-a96f-c8dff3195c05
Pattabiraman, Sundararaghavan
a9f5aac6-6388-4b65-ba29-33aa47aad5a4
Amen, Triana
8dea95c1-8a56-4396-835a-bb7ef5d30ffb
Abraham, Ayelet-chen
9d7bdc49-a883-463d-acce-8635fa88e8b1
Eichler, Noam
ddf58cbc-1616-4704-80fc-65484d21986c
Lyakhovetsky, Roman
dd9f00c5-a583-4a79-a61a-b3088fa6e380
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f

Ogrodnik, Mikołaj, Salmonowicz, Hanna, Brown, Rachel and Kaganovich, Daniel , et al. (2014) Dynamic JUNQ inclusion bodies are asymmetrically inherited in mammalian cell lines through the asymmetric partitioning of vimentin. Proceedings of the National Academy of Sciences of the United States of America, 111 (22), 8049-54. (doi:10.1073/pnas.1324035111).

Record type: Article

Abstract

Aging is associated with the accumulation of several types of damage: in particular, damage to the proteome. Recent work points to a conserved replicative rejuvenation mechanism that works by preventing the inheritance of damaged and misfolded proteins by specific cells during division. Asymmetric inheritance of misfolded and aggregated proteins has been shown in bacteria and yeast, but relatively little evidence exists for a similar mechanism in mammalian cells. Here, we demonstrate, using long-term 4D imaging, that the vimentin intermediate filament establishes mitotic polarity in mammalian cell lines and mediates the asymmetric partitioning of damaged proteins. We show that mammalian JUNQ inclusion bodies containing soluble misfolded proteins are inherited asymmetrically, similarly to JUNQ quality-control inclusions observed in yeast. Mammalian IPOD-like inclusion bodies, meanwhile, are not always inherited by the same cell as the JUNQ. Our study suggests that the mammalian cytoskeleton and intermediate filaments provide the physical scaffold for asymmetric inheritance of dynamic quality-control JUNQ inclusions. Mammalian IPOD inclusions containing amyloidogenic proteins are not partitioned as effectively during mitosis as their counterparts in yeast. These findings provide a valuable mechanistic basis for studying the process of asymmetric inheritance in mammalian cells, including cells potentially undergoing polar divisions, such as differentiating stem cells and cancer cells.

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More information

Published date: 3 June 2014
Keywords: Actins/metabolism, Aging/metabolism, Animals, CHO Cells, Cell Compartmentation/physiology, Cricetulus, HEK293 Cells, HeLa Cells, Humans, Inclusion Bodies/metabolism, Intermediate Filaments/metabolism, Mammals, Mice, Microscopy, Confocal/methods, Mitosis/physiology, Neuroblastoma, Proteasome Endopeptidase Complex/metabolism, Protein Folding, Saccharomyces cerevisiae, Spindle Apparatus/metabolism, Stress, Physiological/physiology, Vimentin/chemistry

Identifiers

Local EPrints ID: 475717
URI: http://eprints.soton.ac.uk/id/eprint/475717
ISSN: 0027-8424
PURE UUID: 896864a1-df09-4f4f-94ea-13830d6353c2
ORCID for Daniel Kaganovich: ORCID iD orcid.org/0000-0003-2398-1596

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Date deposited: 27 Mar 2023 16:30
Last modified: 17 Mar 2024 04:17

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Contributors

Author: Mikołaj Ogrodnik
Author: Hanna Salmonowicz
Author: Rachel Brown
Author: Joanna Turkowska
Author: Władysław Średniawa
Author: Sundararaghavan Pattabiraman
Author: Triana Amen
Author: Ayelet-chen Abraham
Author: Noam Eichler
Author: Roman Lyakhovetsky
Author: Daniel Kaganovich ORCID iD
Corporate Author: et al.

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