ZNF692 organizes a hub specialized in 40S ribosomal subunit maturation enhancing translation in rapidly proliferating cells

M. Carmen Lafita-Navarro; Yi Heng Hao; Chunhui Jiang; Seoyeon Jang; Tsung-Cheng Chang; Isabella N. Brown; Niranjan Venkateswaran; Elizabeth Maurais; Weronika Stachera; Yanfeng Zhang; Dorothy I Mundy; Jungsoo Han; Vanna M. Tran; Marcel Mettlen; Lin Xu; Jeffrey B Woodruff; Nick V Grishin; Lisa Kinch; Joshua T Mendell; Michael Buszczak; Maralice Conacci-Sorrell

doi:10.1016/j.celrep.2023.113280

ZNF692 organizes a hub specialized in 40S ribosomal subunit maturation enhancing translation in rapidly proliferating cells

M. Carmen Lafita-Navarro, Yi Heng Hao, Chunhui Jiang, Seoyeon Jang, Tsung-Cheng Chang, Isabella N. Brown, Niranjan Venkateswaran, Elizabeth Maurais, Weronika Stachera, Yanfeng Zhang, Dorothy I Mundy, Jungsoo Han, Vanna M. Tran, Marcel Mettlen, Lin Xu, Jeffrey B Woodruff, Nick V Grishin, Lisa Kinch, Joshua T Mendell, Michael BuszczakMaralice Conacci-Sorrell

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Increased nucleolar size and activity correlate with aberrant ribosome biogenesis and enhanced translation in cancer cells. One of the first and rate-limiting steps in translation is the interaction of the 40S small ribosome subunit with mRNAs. Here, we report the identification of the zinc finger protein 692 (ZNF692), a MYC-induced nucleolar scaffold that coordinates the final steps in the biogenesis of the small ribosome subunit. ZNF692 forms a hub containing the exosome complex and ribosome biogenesis factors specialized in the final steps of 18S rRNA processing and 40S ribosome maturation in the granular component of the nucleolus. Highly proliferative cells are more reliant on ZNF692 than normal cells; thus, we conclude that effective production of small ribosome subunits is critical for translation efficiency in cancer cells.

Original language	English (US)
Article number	113280
Journal	Cell Reports
Volume	42
Issue number	10
DOIs	https://doi.org/10.1016/j.celrep.2023.113280
State	Published - Oct 31 2023

Keywords

40S
CP: Molecular biology
EXOSC7
EXOSC8
exosome
KRR1
MYC
nucleolus
ribosome biogenesis
rRNA
ZNF692

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.celrep.2023.113280

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Lafita-Navarro, M. C., Hao, Y. H., Jiang, C., Jang, S., Chang, T.-C., Brown, I. N., Venkateswaran, N., Maurais, E., Stachera, W., Zhang, Y., Mundy, D. I., Han, J., Tran, V. M., Mettlen, M., Xu, L., Woodruff, J. B., Grishin, N. V., Kinch, L., Mendell, J. T., ... Conacci-Sorrell, M. (2023). ZNF692 organizes a hub specialized in 40S ribosomal subunit maturation enhancing translation in rapidly proliferating cells. Cell Reports, 42(10), Article 113280. https://doi.org/10.1016/j.celrep.2023.113280

Lafita-Navarro, MC, Hao, YH, Jiang, C, Jang, S, Chang, T-C, Brown, IN, Venkateswaran, N, Maurais, E, Stachera, W, Zhang, Y, Mundy, DI, Han, J, Tran, VM, Mettlen, M , Xu, L , Woodruff, JB , Grishin, NV, Kinch, L, Mendell, JT , Buszczak, M & Conacci-Sorrell, M 2023, 'ZNF692 organizes a hub specialized in 40S ribosomal subunit maturation enhancing translation in rapidly proliferating cells', Cell Reports, vol. 42, no. 10, 113280. https://doi.org/10.1016/j.celrep.2023.113280

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abstract = "Increased nucleolar size and activity correlate with aberrant ribosome biogenesis and enhanced translation in cancer cells. One of the first and rate-limiting steps in translation is the interaction of the 40S small ribosome subunit with mRNAs. Here, we report the identification of the zinc finger protein 692 (ZNF692), a MYC-induced nucleolar scaffold that coordinates the final steps in the biogenesis of the small ribosome subunit. ZNF692 forms a hub containing the exosome complex and ribosome biogenesis factors specialized in the final steps of 18S rRNA processing and 40S ribosome maturation in the granular component of the nucleolus. Highly proliferative cells are more reliant on ZNF692 than normal cells; thus, we conclude that effective production of small ribosome subunits is critical for translation efficiency in cancer cells.",

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author = "Lafita-Navarro, {M. Carmen} and Hao, {Yi Heng} and Chunhui Jiang and Seoyeon Jang and Tsung-Cheng Chang and Brown, {Isabella N.} and Niranjan Venkateswaran and Elizabeth Maurais and Weronika Stachera and Yanfeng Zhang and Mundy, {Dorothy I} and Jungsoo Han and Tran, {Vanna M.} and Marcel Mettlen and Lin Xu and Woodruff, {Jeffrey B} and Grishin, {Nick V} and Lisa Kinch and Mendell, {Joshua T} and Michael Buszczak and Maralice Conacci-Sorrell",

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doi = "10.1016/j.celrep.2023.113280",

language = "English (US)",

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AU - Lafita-Navarro, M. Carmen

AU - Hao, Yi Heng

AU - Jiang, Chunhui

AU - Jang, Seoyeon

AU - Chang, Tsung-Cheng

AU - Brown, Isabella N.

AU - Venkateswaran, Niranjan

AU - Maurais, Elizabeth

AU - Stachera, Weronika

AU - Zhang, Yanfeng

AU - Mundy, Dorothy I

AU - Han, Jungsoo

AU - Tran, Vanna M.

AU - Mettlen, Marcel

AU - Xu, Lin

AU - Woodruff, Jeffrey B

AU - Grishin, Nick V

AU - Kinch, Lisa

AU - Mendell, Joshua T

AU - Buszczak, Michael

AU - Conacci-Sorrell, Maralice

PY - 2023/10/31

Y1 - 2023/10/31

N2 - Increased nucleolar size and activity correlate with aberrant ribosome biogenesis and enhanced translation in cancer cells. One of the first and rate-limiting steps in translation is the interaction of the 40S small ribosome subunit with mRNAs. Here, we report the identification of the zinc finger protein 692 (ZNF692), a MYC-induced nucleolar scaffold that coordinates the final steps in the biogenesis of the small ribosome subunit. ZNF692 forms a hub containing the exosome complex and ribosome biogenesis factors specialized in the final steps of 18S rRNA processing and 40S ribosome maturation in the granular component of the nucleolus. Highly proliferative cells are more reliant on ZNF692 than normal cells; thus, we conclude that effective production of small ribosome subunits is critical for translation efficiency in cancer cells.

AB - Increased nucleolar size and activity correlate with aberrant ribosome biogenesis and enhanced translation in cancer cells. One of the first and rate-limiting steps in translation is the interaction of the 40S small ribosome subunit with mRNAs. Here, we report the identification of the zinc finger protein 692 (ZNF692), a MYC-induced nucleolar scaffold that coordinates the final steps in the biogenesis of the small ribosome subunit. ZNF692 forms a hub containing the exosome complex and ribosome biogenesis factors specialized in the final steps of 18S rRNA processing and 40S ribosome maturation in the granular component of the nucleolus. Highly proliferative cells are more reliant on ZNF692 than normal cells; thus, we conclude that effective production of small ribosome subunits is critical for translation efficiency in cancer cells.

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KW - EXOSC7

KW - EXOSC8

KW - exosome

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KW - MYC

KW - nucleolus

KW - ribosome biogenesis

KW - rRNA

KW - ZNF692

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JO - Cell Reports

JF - Cell Reports

IS - 10

M1 - 113280

ER -

ZNF692 organizes a hub specialized in 40S ribosomal subunit maturation enhancing translation in rapidly proliferating cells

Abstract

Keywords

ASJC Scopus subject areas

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