ATF5 Connects the Pericentriolar Materials to the Proximal End of the Mother Centriole

Bhanupriya Madarampalli; Yunsheng Yuan; Dan Liu; Kathleen Lengel; Yidi Xu; Guangfu Li; Jinming Yang; Xinyuan Liu; Zhimin Lu; David X. Liu

doi:10.1016/j.cell.2015.06.055

ATF5 Connects the Pericentriolar Materials to the Proximal End of the Mother Centriole

Bhanupriya Madarampalli, Yunsheng Yuan, Dan Liu, Kathleen Lengel, Yidi Xu, Guangfu Li, Jinming Yang, Xinyuan Liu, Zhimin Lu, David X. Liu

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

24 Scopus citations

Abstract

Although it is known that the centrioles play instructive roles in pericentriolar material (PCM) assembly and that the PCM is essential for proper centriole formation, the mechanism that governs centriole-PCM interaction is poorly understood. Here, we show that ATF5 forms a characteristic 9-fold symmetrical ring structure in the inner layer of the PCM outfitting the proximal end of the mother centriole. ATF5 controls the centriole-PCM interaction in a cell-cycle- and centriole-age-dependent manner. Interaction of ATF5 with polyglutamylated tubulin (PGT) on the mother centriole and with PCNT in the PCM renders ATF5 as a required molecule in mother centriole-directed PCM accumulation and in PCM-dependent centriole formation. ATF5 depletion blocks PCM accumulation at the centrosome and causes fragmentation of centrioles, leading to the formation of multi-polar mitotic spindles and genomic instability. These data show that ATF5 is an essential structural protein that is required for the interaction between the mother centriole and the PCM.

Original language	English
Pages (from-to)	580-592
Number of pages	13
Journal	Cell
Volume	162
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2015.06.055
State	Published - Aug 1 2015

Bibliographical note

Funding Information:
We thank B. Stanley, A. Stanley, and J. Dai for help with mass spectrometry analysis and R. Myers for help with electron microscopy. We thank J. Angelastro, P. Baas, S. Doxsey, M. Green, L. Greene, L. Mourey, J. Rattner, O. Semmes, and R. Vallee for providing valuable reagents. We thank T. Denton and Z. Xia for expert consultation on synthesis of EDC-activated polyglutamate- and polylysinate-conjugated tubulin. We also thank Edward Liu for helping draw the Graphical Abstract for this manuscript. This work was supported in part by grants from the American Cancer Society and the U.S. Department of Defense (to D.X.L.).

Publisher Copyright:
© 2015 Elsevier Inc.

Keywords

ATF5
PCM
PCNT
centriole
centrosome
genomic instability
mitotic spindle
polyglutamylated tubulin

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology (all)

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10.1016/j.cell.2015.06.055

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title = "ATF5 Connects the Pericentriolar Materials to the Proximal End of the Mother Centriole",

abstract = "Although it is known that the centrioles play instructive roles in pericentriolar material (PCM) assembly and that the PCM is essential for proper centriole formation, the mechanism that governs centriole-PCM interaction is poorly understood. Here, we show that ATF5 forms a characteristic 9-fold symmetrical ring structure in the inner layer of the PCM outfitting the proximal end of the mother centriole. ATF5 controls the centriole-PCM interaction in a cell-cycle- and centriole-age-dependent manner. Interaction of ATF5 with polyglutamylated tubulin (PGT) on the mother centriole and with PCNT in the PCM renders ATF5 as a required molecule in mother centriole-directed PCM accumulation and in PCM-dependent centriole formation. ATF5 depletion blocks PCM accumulation at the centrosome and causes fragmentation of centrioles, leading to the formation of multi-polar mitotic spindles and genomic instability. These data show that ATF5 is an essential structural protein that is required for the interaction between the mother centriole and the PCM.",

keywords = "ATF5, PCM, PCNT, centriole, centrosome, genomic instability, mitotic spindle, polyglutamylated tubulin",

author = "Bhanupriya Madarampalli and Yunsheng Yuan and Dan Liu and Kathleen Lengel and Yidi Xu and Guangfu Li and Jinming Yang and Xinyuan Liu and Zhimin Lu and Liu, {David X.}",

note = "Funding Information: We thank B. Stanley, A. Stanley, and J. Dai for help with mass spectrometry analysis and R. Myers for help with electron microscopy. We thank J. Angelastro, P. Baas, S. Doxsey, M. Green, L. Greene, L. Mourey, J. Rattner, O. Semmes, and R. Vallee for providing valuable reagents. We thank T. Denton and Z. Xia for expert consultation on synthesis of EDC-activated polyglutamate- and polylysinate-conjugated tubulin. We also thank Edward Liu for helping draw the Graphical Abstract for this manuscript. This work was supported in part by grants from the American Cancer Society and the U.S. Department of Defense (to D.X.L.). Publisher Copyright: {\textcopyright} 2015 Elsevier Inc.",

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AU - Xu, Yidi

AU - Li, Guangfu

AU - Yang, Jinming

AU - Liu, Xinyuan

AU - Lu, Zhimin

AU - Liu, David X.

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AB - Although it is known that the centrioles play instructive roles in pericentriolar material (PCM) assembly and that the PCM is essential for proper centriole formation, the mechanism that governs centriole-PCM interaction is poorly understood. Here, we show that ATF5 forms a characteristic 9-fold symmetrical ring structure in the inner layer of the PCM outfitting the proximal end of the mother centriole. ATF5 controls the centriole-PCM interaction in a cell-cycle- and centriole-age-dependent manner. Interaction of ATF5 with polyglutamylated tubulin (PGT) on the mother centriole and with PCNT in the PCM renders ATF5 as a required molecule in mother centriole-directed PCM accumulation and in PCM-dependent centriole formation. ATF5 depletion blocks PCM accumulation at the centrosome and causes fragmentation of centrioles, leading to the formation of multi-polar mitotic spindles and genomic instability. These data show that ATF5 is an essential structural protein that is required for the interaction between the mother centriole and the PCM.

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ATF5 Connects the Pericentriolar Materials to the Proximal End of the Mother Centriole

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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