K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution. / Suryo Rahmanto, Aldwin; Blum, Christian J.; Scalera, Claudia; Heidelberger, Jan B.; Mesitov, Mikhail; Horn-Ghetko, Daniel; Gräf, Justus F.; Mikicic, Ivan; Hobrecht, Rebecca; Orekhova, Anna; Ostermaier, Matthias; Ebersberger, Stefanie; Möckel, Martin M.; Krapoth, Nils; Da Silva Fernandes, Nádia; Mizi, Athanasia; Zhu, Yajie; Chen, Jia Xuan; Choudhary, Chunaram; Papantonis, Argyris; Ulrich, Helle D.; Schulman, Brenda A.; König, Julian; Beli, Petra.

In: Molecular Cell, Vol. 83, No. 23, 2023, p. 4272-4289.e10.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Suryo Rahmanto, A, Blum, CJ, Scalera, C, Heidelberger, JB, Mesitov, M, Horn-Ghetko, D, Gräf, JF, Mikicic, I, Hobrecht, R, Orekhova, A, Ostermaier, M, Ebersberger, S, Möckel, MM, Krapoth, N, Da Silva Fernandes, N, Mizi, A, Zhu, Y, Chen, JX, Choudhary, C, Papantonis, A, Ulrich, HD, Schulman, BA, König, J & Beli, P 2023, 'K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution', Molecular Cell, vol. 83, no. 23, pp. 4272-4289.e10. https://doi.org/10.1016/j.molcel.2023.10.011

APA

Suryo Rahmanto, A., Blum, C. J., Scalera, C., Heidelberger, J. B., Mesitov, M., Horn-Ghetko, D., Gräf, J. F., Mikicic, I., Hobrecht, R., Orekhova, A., Ostermaier, M., Ebersberger, S., Möckel, M. M., Krapoth, N., Da Silva Fernandes, N., Mizi, A., Zhu, Y., Chen, J. X., Choudhary, C., ... Beli, P. (2023). K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution. Molecular Cell, 83(23), 4272-4289.e10. https://doi.org/10.1016/j.molcel.2023.10.011

Vancouver

Suryo Rahmanto A, Blum CJ, Scalera C, Heidelberger JB, Mesitov M, Horn-Ghetko D et al. K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution. Molecular Cell. 2023;83(23):4272-4289.e10. https://doi.org/10.1016/j.molcel.2023.10.011

Author

Suryo Rahmanto, Aldwin ; Blum, Christian J. ; Scalera, Claudia ; Heidelberger, Jan B. ; Mesitov, Mikhail ; Horn-Ghetko, Daniel ; Gräf, Justus F. ; Mikicic, Ivan ; Hobrecht, Rebecca ; Orekhova, Anna ; Ostermaier, Matthias ; Ebersberger, Stefanie ; Möckel, Martin M. ; Krapoth, Nils ; Da Silva Fernandes, Nádia ; Mizi, Athanasia ; Zhu, Yajie ; Chen, Jia Xuan ; Choudhary, Chunaram ; Papantonis, Argyris ; Ulrich, Helle D. ; Schulman, Brenda A. ; König, Julian ; Beli, Petra. / K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution. In: Molecular Cell. 2023 ; Vol. 83, No. 23. pp. 4272-4289.e10.

Bibtex

@article{9c082a5066554360a8906dbd30b90ef7,
title = "K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution",
abstract = "Reactive aldehydes are produced by normal cellular metabolism or after alcohol consumption, and they accumulate in human tissues if aldehyde clearance mechanisms are impaired. Their toxicity has been attributed to the damage they cause to genomic DNA and the subsequent inhibition of transcription and replication. However, whether interference with other cellular processes contributes to aldehyde toxicity has not been investigated. We demonstrate that formaldehyde induces RNA-protein crosslinks (RPCs) that stall the ribosome and inhibit translation in human cells. RPCs in the messenger RNA (mRNA) are recognized by the translating ribosomes, marked by atypical K6-linked ubiquitylation catalyzed by the RING-in-between-RING (RBR) E3 ligase RNF14, and subsequently resolved by the ubiquitin- and ATP-dependent unfoldase VCP. Our findings uncover an evolutionary conserved formaldehyde-induced stress response pathway that protects cells against RPC accumulation in the cytoplasm, and they suggest that RPCs contribute to the cellular and tissue toxicity of reactive aldehydes.",
keywords = "K6-linked ubiquitylation, quantitative proteomics, reactive aldehydes, ribosome, RNA-protein crosslinks, RNF14, translation, VCP",
author = "{Suryo Rahmanto}, Aldwin and Blum, {Christian J.} and Claudia Scalera and Heidelberger, {Jan B.} and Mikhail Mesitov and Daniel Horn-Ghetko and Gr{\"a}f, {Justus F.} and Ivan Mikicic and Rebecca Hobrecht and Anna Orekhova and Matthias Ostermaier and Stefanie Ebersberger and M{\"o}ckel, {Martin M.} and Nils Krapoth and {Da Silva Fernandes}, N{\'a}dia and Athanasia Mizi and Yajie Zhu and Chen, {Jia Xuan} and Chunaram Choudhary and Argyris Papantonis and Ulrich, {Helle D.} and Schulman, {Brenda A.} and Julian K{\"o}nig and Petra Beli",
note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",
year = "2023",
doi = "10.1016/j.molcel.2023.10.011",
language = "English",
volume = "83",
pages = "4272--4289.e10",
journal = "Molecular Cell",
issn = "1097-2765",
publisher = "Cell Press",
number = "23",

}

RIS

TY - JOUR

T1 - K6-linked ubiquitylation marks formaldehyde-induced RNA-protein crosslinks for resolution

AU - Suryo Rahmanto, Aldwin

AU - Blum, Christian J.

AU - Scalera, Claudia

AU - Heidelberger, Jan B.

AU - Mesitov, Mikhail

AU - Horn-Ghetko, Daniel

AU - Gräf, Justus F.

AU - Mikicic, Ivan

AU - Hobrecht, Rebecca

AU - Orekhova, Anna

AU - Ostermaier, Matthias

AU - Ebersberger, Stefanie

AU - Möckel, Martin M.

AU - Krapoth, Nils

AU - Da Silva Fernandes, Nádia

AU - Mizi, Athanasia

AU - Zhu, Yajie

AU - Chen, Jia Xuan

AU - Choudhary, Chunaram

AU - Papantonis, Argyris

AU - Ulrich, Helle D.

AU - Schulman, Brenda A.

AU - König, Julian

AU - Beli, Petra

N1 - Publisher Copyright: © 2023 The Author(s)

PY - 2023

Y1 - 2023

N2 - Reactive aldehydes are produced by normal cellular metabolism or after alcohol consumption, and they accumulate in human tissues if aldehyde clearance mechanisms are impaired. Their toxicity has been attributed to the damage they cause to genomic DNA and the subsequent inhibition of transcription and replication. However, whether interference with other cellular processes contributes to aldehyde toxicity has not been investigated. We demonstrate that formaldehyde induces RNA-protein crosslinks (RPCs) that stall the ribosome and inhibit translation in human cells. RPCs in the messenger RNA (mRNA) are recognized by the translating ribosomes, marked by atypical K6-linked ubiquitylation catalyzed by the RING-in-between-RING (RBR) E3 ligase RNF14, and subsequently resolved by the ubiquitin- and ATP-dependent unfoldase VCP. Our findings uncover an evolutionary conserved formaldehyde-induced stress response pathway that protects cells against RPC accumulation in the cytoplasm, and they suggest that RPCs contribute to the cellular and tissue toxicity of reactive aldehydes.

AB - Reactive aldehydes are produced by normal cellular metabolism or after alcohol consumption, and they accumulate in human tissues if aldehyde clearance mechanisms are impaired. Their toxicity has been attributed to the damage they cause to genomic DNA and the subsequent inhibition of transcription and replication. However, whether interference with other cellular processes contributes to aldehyde toxicity has not been investigated. We demonstrate that formaldehyde induces RNA-protein crosslinks (RPCs) that stall the ribosome and inhibit translation in human cells. RPCs in the messenger RNA (mRNA) are recognized by the translating ribosomes, marked by atypical K6-linked ubiquitylation catalyzed by the RING-in-between-RING (RBR) E3 ligase RNF14, and subsequently resolved by the ubiquitin- and ATP-dependent unfoldase VCP. Our findings uncover an evolutionary conserved formaldehyde-induced stress response pathway that protects cells against RPC accumulation in the cytoplasm, and they suggest that RPCs contribute to the cellular and tissue toxicity of reactive aldehydes.

KW - K6-linked ubiquitylation

KW - quantitative proteomics

KW - reactive aldehydes

KW - ribosome

KW - RNA-protein crosslinks

KW - RNF14

KW - translation

KW - VCP

U2 - 10.1016/j.molcel.2023.10.011

DO - 10.1016/j.molcel.2023.10.011

M3 - Journal article

C2 - 37951215

AN - SCOPUS:85178169389

VL - 83

SP - 4272-4289.e10

JO - Molecular Cell

JF - Molecular Cell

SN - 1097-2765

IS - 23

ER -

ID: 378949358