Molecular architecture of a cylindrical self-assembly at human centrosomes

Kim, Tae-Sung; Zhang, Liang; Ahn, Jong il; Meng, Lingjun; Chen, Yang; Lee, Eunhye; Bang, Jeong Kyu; Lim, Jung Mi; Ghirlando, Rodolfo; Fan, Lixin; Wang, Yun-Xing; Kim, Bo Yeon; Park, Jung-Eun; Lee, Kyung S.

doi:10.1038/s41467-019-08838-2

Molecular architecture of a cylindrical self-assembly at human centrosomes

Journal Article · Mon Mar 11 00:00:00 EDT 2019 · Nature Communications

DOI:https://doi.org/10.1038/s41467-019-08838-2· OSTI ID:1502246

^[1]; ^[1]; ^[1]; Meng, Lingjun ^[1]; Chen, Yang ^[1]; Lee, Eunhye ^[1]; ^[2]; Lim, Jung Mi ^[1]; Ghirlando, Rodolfo ^[3]; Fan, Lixin ^[4]; Wang, Yun-Xing ^[1]; ^[5]; ^[1]; ^[1]

National Cancer Inst., Bethesda, MD (United States)
Korea Basic Science Inst., Ochang (Korea)
National Inst. of Health (NIH), Bethesda, MD (United States). National Inst. of Diabetes, Digestive and Kidney Diseases (NIDDK)
Frederick National Lab. for Cancer Research, MD (United States)
Korea Research Inst. of Bioscience and Biotechnology, Ochang (Republic of Korea)

The cell is constructed by higher-order structures and organelles through complex interactions among distinct structural constituents. The centrosome is a membraneless organelle composed of two microtubule-derived structures called centrioles and an amorphous mass of pericentriolar material. Super-resolution microscopic analyses in various organisms revealed that diverse pericentriolar material proteins are concentrically localized around a centriole in a highly organized manner. However, the molecular nature underlying these organizations remains unknown. Here we show that two human pericentriolar material scaffolds, Cep63 and Cep152, cooperatively generate a heterotetrameric α-helical bundle that functions in conjunction with its neighboring hydrophobic motifs to self-assemble into a higher-order cylindrical architecture capable of recruiting downstream components, including Plk4, a key regulator for centriole duplication. Mutations disrupting the self-assembly abrogate Plk4-mediated centriole duplication. Because pericentriolar material organization is evolutionarily conserved, this work may offer a paradigm for investigating the assembly and function of centrosomal scaffolds in various organisms.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Eunice Kennedy Shriver National Institute for Child Health & Human Development (NICHD); National Cancer Institute (NCI); National Institute of Diabetes, Digestive and Kidney Diseases (NIDDK); National Research Council of Science and Technology (NST)

OSTI ID:: 1502246

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (71)

Structural Basis of the 9-Fold Symmetry of Centrioles Kitagawa, Daiju; Vakonakis, Ioannis; Olieric, Natacha Cell, Vol. 144, Issue 3 https://doi.org/10.1016/j.cell.2011.01.008	journal	February 2011
The Centrosome Is a Selective Condensate that Nucleates Microtubules by Concentrating Tubulin Woodruff, Jeffrey B.; Ferreira Gomes, Beatriz; Widlund, Per O. Cell, Vol. 169, Issue 6 https://doi.org/10.1016/j.cell.2017.05.028	journal	June 2017
Selective Chemical Crosslinking Reveals a Cep57-Cep63-Cep152 Centrosomal Complex Lukinavičius, Gražvydas; Lavogina, Darja; Orpinell, Meritxell Current Biology, Vol. 23, Issue 3 https://doi.org/10.1016/j.cub.2012.12.030	journal	February 2013
Coiled Coils – A Model System for the 21st Century Lupas, Andrei N.; Bassler, Jens Trends in Biochemical Sciences, Vol. 42, Issue 2 https://doi.org/10.1016/j.tibs.2016.10.007	journal	February 2017
Analytical Ultracentrifugation: Sedimentation Velocity and Sedimentation Equilibrium Cole, James L.; Lary, Jeffrey W.; Moody, Thomas P. Biophysical Tools for Biologists, Volume One: In Vitro Techniques, p. 143-179 https://doi.org/10.1016/s0091-679x(07)84006-4	book	January 2008
A Polo Match for Plk1 Leung, Genie C.; Sicheri, Frank Cell, Vol. 115, Issue 1 https://doi.org/10.1016/s0092-8674(03)00761-x	journal	October 2003
Subdiffraction-resolution fluorescence microscopy reveals a domain of the centrosome critical for pericentriolar material organization Mennella, V.; Keszthelyi, B.; McDonald, K. L. Nature Cell Biology, Vol. 14, Issue 11 https://doi.org/10.1038/ncb2597	journal	October 2012
The Cep63 paralogue Deup1 enables massive de novo centriole biogenesis for vertebrate multiciliogenesis Zhao, Huijie; Zhu, Lei; Zhu, Yunlu Nature Cell Biology, Vol. 15, Issue 12 https://doi.org/10.1038/ncb2880	journal	November 2013
Direct interaction of Plk4 with STIL ensures formation of a single procentriole per parental centriole Ohta, Midori; Ashikawa, Tomoko; Nozaki, Yuka Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6267	journal	October 2014
CEP152 is a genome maintenance protein disrupted in Seckel syndrome Kalay, Ersan; Yigit, Gökhan; Aslan, Yakup Nature Genetics, Vol. 43, Issue 1 https://doi.org/10.1038/ng.725	journal	December 2010
A primary microcephaly protein complex forms a ring around parental centrioles Sir, Joo-Hee; Barr, Alexis R.; Nicholas, Adeline K. Nature Genetics, Vol. 43, Issue 11 https://doi.org/10.1038/ng.971	journal	October 2011
Centrosomes and cancer: revisiting a long-standing relationship Gönczy, Pierre Nature Reviews Cancer, Vol. 15, Issue 11 https://doi.org/10.1038/nrc3995	journal	October 2015
Polo-like kinases: structural variations lead to multiple functions Zitouni, Sihem; Nabais, Catarina; Jana, Swadhin Chandra Nature Reviews Molecular Cell Biology, Vol. 15, Issue 7 https://doi.org/10.1038/nrm3819	journal	June 2014
Centrosome function and assembly in animal cells Conduit, Paul T.; Wainman, Alan; Raff, Jordan W. Nature Reviews Molecular Cell Biology, Vol. 16, Issue 10 https://doi.org/10.1038/nrm4062	journal	September 2015
Molecular basis for unidirectional scaffold switching of human Plk4 in centriole biogenesis Park, Suk-Youl; Park, Jung-Eun; Kim, Tae-Sung Nature Structural & Molecular Biology, Vol. 21, Issue 8 https://doi.org/10.1038/nsmb.2846	journal	June 2014
The PLK4–STIL–SAS-6 module at the core of centriole duplication Arquint, Christian; Nigg, Erich A. Biochemical Society Transactions, Vol. 44, Issue 5 https://doi.org/10.1042/bst20160116	journal	October 2016
Hierarchical recruitment of Plk4 and regulation of centriole biogenesis by two centrosomal scaffolds, Cep192 and Cep152 Kim, T. -S.; Park, J. -E.; Shukla, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1319656110	journal	November 2013
Cep152 interacts with Plk4 and is required for centriole duplication Hatch, Emily M.; Kulukian, Anita; Holland, Andrew J. The Journal of Cell Biology, Vol. 191, Issue 4 https://doi.org/10.1083/jcb.201006049	journal	November 2010
Cep152 acts as a scaffold for recruitment of Plk4 and CPAP to the centrosome Cizmecioglu, Onur; Arnold, Marc; Bahtz, Ramona The Journal of Cell Biology, Vol. 191, Issue 4 https://doi.org/10.1083/jcb.201007107	journal	November 2010
The Protein Phosphatase 2A regulatory subunit Twins stabilizes Plk4 to induce centriole amplification Brownlee, Christopher W.; Klebba, Joey E.; Buster, Daniel W. The Journal of Cell Biology, Vol. 195, Issue 2 https://doi.org/10.1083/jcb.201107086	journal	October 2011
Mechanisms of HsSAS-6 assembly promoting centriole formation in human cells Keller, Debora; Orpinell, Meritxell; Olivier, Nicolas The Journal of Cell Biology, Vol. 204, Issue 5 https://doi.org/10.1083/jcb.201307049	journal	March 2014
Structured illumination of the interface between centriole and peri-centriolar material Fu, Jingyan; Glover, David M. Open Biology, Vol. 2, Issue 8 https://doi.org/10.1098/rsob.120104	journal	August 2012
The Centrosome and Its Duplication Cycle Fu, Jingyan; Hagan, Iain M.; Glover, David M. Cold Spring Harbor Perspectives in Biology, Vol. 7, Issue 2 https://doi.org/10.1101/cshperspect.a015800	journal	February 2015
The Centrosome, a Multitalented Renaissance Organelle Vertii, Anastassiia; Hehnly, Heidi; Doxsey, Stephen Cold Spring Harbor Perspectives in Biology, Vol. 8, Issue 12 https://doi.org/10.1101/cshperspect.a025049	journal	December 2016
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/s0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/s0907444904019158	journal	November 2004
Structural Plasticity in Actin and Tubulin Polymer Dynamics Kueh, H. Y.; Mitchison, T. J. Science, Vol. 325, Issue 5943 https://doi.org/10.1126/science.1168823	journal	August 2009
Geometric Cue for Protein Localization in a Bacterium Ramamurthi, K. S.; Lecuyer, S.; Stone, H. A. Science, Vol. 323, Issue 5919 https://doi.org/10.1126/science.1169218	journal	March 2009
Predicting coiled coils from protein sequences Lupas, A.; Van Dyke, M.; Stock, J. Science, Vol. 252, Issue 5009, p. 1162-1164 https://doi.org/10.1126/science.252.5009.1162	journal	May 1991
Regulated assembly of a supramolecular centrosome scaffold in vitro Woodruff, J. B.; Wueseke, O.; Viscardi, V. Science, Vol. 348, Issue 6236 https://doi.org/10.1126/science.aaa3923	journal	May 2015
Centriole Biogenesis: From Identifying the Characters to Understanding the Plot Banterle, Niccolò; Gönczy, Pierre Annual Review of Cell and Developmental Biology, Vol. 33, Issue 1 https://doi.org/10.1146/annurev-cellbio-100616-060454	journal	October 2017
3D-structured illumination microscopy provides novel insight into architecture of human centrosomes Sonnen, Katharina F.; Schermelleh, Lothar; Leonhardt, Heinrich Biology Open, Vol. 1, Issue 10 https://doi.org/10.1242/bio.20122337	journal	August 2012
Plk4-dependent phosphorylation of STIL is required for centriole duplication Kratz, A. -S.; Barenz, F.; Richter, K. T. Biology Open, Vol. 4, Issue 3 https://doi.org/10.1242/bio.201411023	journal	February 2015
Advances in fluorescent protein technology Shaner, N. C.; Patterson, G. H.; Davidson, M. W. Journal of Cell Science, Vol. 120, Issue 24 https://doi.org/10.1242/jcs.005801	journal	December 2007
Cell-cycle-regulated expression of STIL controls centriole number in human cells Arquint, C.; Sonnen, K. F.; Stierhof, Y. -D. Journal of Cell Science, Vol. 125, Issue 5 https://doi.org/10.1242/jcs.099887	journal	February 2012
STIL is required for centriole duplication in human cells Vulprecht, J.; David, A.; Tibelius, A. Journal of Cell Science, Vol. 125, Issue 5 https://doi.org/10.1242/jcs.104109	journal	February 2012
Resolution Doubling in 3D-STORM Imaging through Improved Buffers Olivier, Nicolas; Keller, Debora; Gönczy, Pierre PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069004	journal	July 2013
Structural Basis for Mitotic Centrosome Assembly in Flies. Feng, Zhe; Caballe, Anna; Wainman, Alan Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.10292	text	January 2017
Overview of Current Methods in Sedimentation Velocity and Sedimentation Equilibrium Analytical Ultracentrifugation Zhao, Huaying; Brautigam, Chad A.; Ghirlando, Rodolfo Current Protocols in Protein Science, Vol. 71, Issue 1 https://doi.org/10.1002/0471140864.ps2012s71	journal	February 2013
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Analytical Ultracentrifugation: Sedimentation Velocity and Sedimentation Equilibrium Cole, James L.; Lary, Jeffrey W.; Moody, Thomas P. Biophysical Tools for Biologists, Volume One: In Vitro Techniques, p. 143-179 https://doi.org/10.1016/S0091-679X(07)84006-4	book	January 2008
The Molecular Basis for Phosphodependent Substrate Targeting and Regulation of Plks by the Polo-Box Domain Elia, Andrew E. H.; Rellos, Peter; Haire, Lesley F. Cell, Vol. 115, Issue 1 https://doi.org/10.1016/S0092-8674(03)00725-6	journal	October 2003
Structural Basis for Mitotic Centrosome Assembly in Flies Feng, Zhe; Caballe, Anna; Wainman, Alan Cell, Vol. 169, Issue 6 https://doi.org/10.1016/j.cell.2017.05.030	journal	June 2017
Asterless Licenses Daughter Centrioles to Duplicate for the First Time in Drosophila Embryos Novak, Zsofia A.; Conduit, Paul T.; Wainman, Alan Current Biology, Vol. 24, Issue 11 https://doi.org/10.1016/j.cub.2014.04.023	journal	June 2014
Principles of Protein−Protein Interactions: What are the Preferred Ways For Proteins To Interact? Keskin, Ozlem; Gursoy, Attila; Ma, Buyong Chemical Reviews, Vol. 108, Issue 4 https://doi.org/10.1021/cr040409x	journal	April 2008
The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation: STIL is required for procentriole formation Tang, Chieh-Ju C.; Lin, Shin-Yi; Hsu, Wen-Bin The EMBO Journal, Vol. 30, Issue 23 https://doi.org/10.1038/emboj.2011.378	journal	October 2011
Interfaces and the driving force of hydrophobic assembly Chandler, David Nature, Vol. 437, Issue 7059 https://doi.org/10.1038/nature04162	journal	September 2005
Subdiffraction imaging of centrosomes reveals higher-order organizational features of pericentriolar material Lawo, Steffen; Hasegan, Monica; Gupta, Gagan D. Nature Cell Biology, Vol. 14, Issue 11 https://doi.org/10.1038/ncb2591	journal	October 2012
CEP63 deficiency promotes p53-dependent microcephaly and reveals a role for the centrosome in meiotic recombination Marjanović, Marko; Sánchez-Huertas, Carlos; Terré, Berta Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8676	journal	July 2015
Once and only once: mechanisms of centriole duplication and their deregulation in disease Nigg, Erich A.; Holland, Andrew J. Nature Reviews Molecular Cell Biology, Vol. 19, Issue 5 https://doi.org/10.1038/nrm.2017.127	journal	January 2018
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
The PLK4–STIL–SAS-6 module at the core of centriole duplication Arquint, Christian; Nigg, Erich A. Biochemical Society Transactions, Vol. 44, Issue 5 https://doi.org/10.1042/BST20160116	journal	October 2016
Binding of STIL to Plk4 activates kinase activity to promote centriole assembly Moyer, Tyler C.; Clutario, Kevin M.; Lambrus, Bramwell G. The Journal of Cell Biology, Vol. 209, Issue 6 https://doi.org/10.1083/jcb.201502088	journal	June 2015
Phosphatidylserine dynamics in cellular membranes Kay, Jason G.; Koivusalo, Mirkka; Ma, Xiaoxiao Molecular Biology of the Cell, Vol. 23, Issue 11 https://doi.org/10.1091/mbc.e11-11-0936	journal	June 2012
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Plk is an M-phase-specific protein kinase and interacts with a kinesin-like protein, CHO1/MKLP-1. Lee, K. S.; Yuan, Y. L.; Kuriyama, R. Molecular and Cellular Biology, Vol. 15, Issue 12 https://doi.org/10.1128/MCB.15.12.7143	journal	December 1995
High-efficiency transformation of mammalian cells by plasmid DNA. Chen, C.; Okayama, H. Molecular and Cellular Biology, Vol. 7, Issue 8 https://doi.org/10.1128/MCB.7.8.2745	journal	August 1987
High-efficiency transformation of mammalian cells by plasmid DNA Chen, C.; Okayama, H. Molecular and Cellular Biology, Vol. 7, Issue 8 https://doi.org/10.1128/mcb.7.8.2745-2752.1987	journal	August 1987
Advances in fluorescent protein technology Shaner, Nathan C.; Patterson, George H.; Davidson, Michael W. Journal of Cell Science, Vol. 124, Issue 13 https://doi.org/10.1242/jcs.094722	journal	July 2011
Human Cep192 and Cep152 cooperate in Plk4 recruitment and centriole duplication Sonnen, K. F.; Gabryjonczyk, A. -M.; Anselm, E. Journal of Cell Science, Vol. 126, Issue 14 https://doi.org/10.1242/jcs.129502	journal	May 2013
Cep63 and Cep152 Cooperate to Ensure Centriole Duplication Brown, Nicola J.; Marjanović, Marko; Lüders, Jens PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069986	journal	July 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
Structural Basis for Mitotic Centrosome Assembly in Flies Feng, Zhe; Caballe, Anna; Wainman, Alan Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2017-13517	text	January 2017
CEP152 is a genome maintenance protein disrupted in Seckel syndrome Kalay, E.; Al, Et; Rauch, A. Nature Publishing Group https://doi.org/10.5167/uzh-47631	text	January 2011
Centriolar satellites assemble centrosomal microcephaly proteins to recruit CDK2 and promote centriole duplication Kodani, Andrew; Yu, Timothy W.; Johnson, Jeffrey R. eLife, Vol. 4 https://doi.org/10.7554/eLife.07519	journal	August 2015

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