Self-assembly of pericentriolar material in interphase cells lacking centrioles

Fangrui Chen; Jingchao Wu; Malina K Iwanski; Daphne Jurriens; Arianna Sandron; Milena Pasolli; Gianmarco Puma; Jannes Z Kromhout; Chao Yang; Wilco Nijenhuis; Lukas C Kapitein; Florian Berger; Anna Akhmanova

doi:10.7554/eLife.77892

Self-assembly of pericentriolar material in interphase cells lacking centrioles

Fangrui Chen, Jingchao Wu, Malina K Iwanski, Daphne Jurriens, Arianna Sandron, Milena Pasolli, Gianmarco Puma, Jannes Z Kromhout, Chao Yang, Wilco Nijenhuis, Lukas C Kapitein, Florian Berger, Anna Akhmanova

Utrecht University of Applied Sciences

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

Abstract

The major microtubule-organizing center (MTOC) in animal cells, the centrosome, comprises a pair of centrioles surrounded by pericentriolar material (PCM), which nucleates and anchors microtubules. Centrosome assembly depends on PCM binding to centrioles, PCM self-association and dynein-mediated PCM transport, but the self-assembly properties of PCM components in interphase cells are poorly understood. Here, we used experiments and modeling to study centriole18 independent features of interphase PCM assembly. We showed that when centrioles are lost due to PLK4 depletion or inhibition, dynein-based transport and self-clustering of PCM proteins are sufficient to form a single compact MTOC, which generates a dense radial microtubule array. Interphase self-assembly of PCM components depends on γ-tubulin, pericentrin, CDK5RAP2 and ninein, but not NEDD1, CEP152 or CEP192. Formation of a compact acentriolar MTOC is inhibited by AKAP450-dependent PCM recruitment to the Golgi or by randomly organized CAMSAP2-stabilized microtubules, which keep PCM mobile and prevent its coalescence. Linking of CAMSAP2 to a minus25 end-directed motor leads to the formation of an MTOC, but MTOC compaction requires cooperation with pericentrin-containing self-clustering PCM. Our data reveal that interphase PCM contains a set of components that can self-assemble into a compact structure and organize microtubules, but PCM self-organization is sensitive to motor- and microtubule-based rearrangement.

Original language	English
Article number	e77892
Pages (from-to)	1-47
Journal	eLife
Volume	11
DOIs	https://doi.org/10.7554/eLife.77892
Publication status	Published - 5 Jul 2022

Bibliographical note

Funding Information:
We thank Lynne Cassimeris (Lehigh University, USA), Pierre Gönczy and Didier Trono (EPFL, Switzerland), Dr. Duane Compton (Geisel School of Medicine at Dartmouth, USA) and Dr. Laurence Pelletier (Lunenfeld-Tanenbaum Research Institute, Canada) for the gift of materials and Ilya Grigoriev and Eugene Katrukha (Biology Imaging Center, Utrecht University) for the help with imaging and image analysis. This work was supported by China Scholarship Council scholarships to Fangrui Chen, Jingchao Wu and Chao Yang, the Netherlands Organization for Scientific Research Spinoza prize to A.A, as well as the European Research Council Consolidator Grant 819219 to L.C.K. and the Eindhoven-Wageningen-Utrecht Alliance (www.ewuu.nl) that supports the Center for Living Technologies.

Funding Information:
We?thank?Lynne?Cassimeris?(Lehigh?University,?USA),?Pierre?Gönczy?and?Didier?Trono?(EPFL,? Switzerland),?Dr.?Duane?Compton?(Geisel?School?of?Medicine?at?Dartmouth,?USA)?and?Dr.?Laurence? Pelletier?(Lunenfeld‐Tanenbaum?Research?Institute,?Canada)?for?the?gift?of?materials?and?Ilya? Grigoriev?and?Eugene?Katrukha?(Biology?Imaging?Center,?Utrecht?University)?for?the?help?with? imaging?and?image?analysis.?This?work?was?supported?by?China?Scholarship?Council?scholarships?to? Fangrui?Chen,?Jingchao?Wu?and?Chao?Yang,?the?Netherlands?Organization?for?Scientific?Research? Spinoza?prize?to?A.A,?as?well?as?the?European?Research?Council?Consolidator?Grant?819219?to?L.C.K.? and?the?Eindhoven‐Wageningen‐Utrecht?Alliance?(www.ewuu.nl)?that?supports?the?Center?for?Living? Technologies.?

Publisher Copyright:
© 2022, eLife Sciences Publications Ltd. All rights reserved.

Keywords

Animals
Centrioles/metabolism
Centrosome/metabolism
Dyneins/metabolism
Interphase
Microtubules/metabolism
Human
PLK4
pericentrin
microtubule-organizing center
pericentriolar material
centrosome
dynein
microtubule
CAMSAP

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title = "Self-assembly of pericentriolar material in interphase cells lacking centrioles",

abstract = "The major microtubule-organizing center (MTOC) in animal cells, the centrosome, comprises a pair of centrioles surrounded by pericentriolar material (PCM), which nucleates and anchors microtubules. Centrosome assembly depends on PCM binding to centrioles, PCM self-association and dynein-mediated PCM transport, but the self-assembly properties of PCM components in interphase cells are poorly understood. Here, we used experiments and modeling to study centriole18 independent features of interphase PCM assembly. We showed that when centrioles are lost due to PLK4 depletion or inhibition, dynein-based transport and self-clustering of PCM proteins are sufficient to form a single compact MTOC, which generates a dense radial microtubule array. Interphase self-assembly of PCM components depends on γ-tubulin, pericentrin, CDK5RAP2 and ninein, but not NEDD1, CEP152 or CEP192. Formation of a compact acentriolar MTOC is inhibited by AKAP450-dependent PCM recruitment to the Golgi or by randomly organized CAMSAP2-stabilized microtubules, which keep PCM mobile and prevent its coalescence. Linking of CAMSAP2 to a minus25 end-directed motor leads to the formation of an MTOC, but MTOC compaction requires cooperation with pericentrin-containing self-clustering PCM. Our data reveal that interphase PCM contains a set of components that can self-assemble into a compact structure and organize microtubules, but PCM self-organization is sensitive to motor- and microtubule-based rearrangement.",

keywords = "Animals, Centrioles/metabolism, Centrosome/metabolism, Dyneins/metabolism, Interphase, Microtubules/metabolism, Human, PLK4, pericentrin, microtubule-organizing center, pericentriolar material, centrosome, dynein, microtubule, CAMSAP",

author = "Fangrui Chen and Jingchao Wu and Iwanski, \{Malina K\} and Daphne Jurriens and Arianna Sandron and Milena Pasolli and Gianmarco Puma and Kromhout, \{Jannes Z\} and Chao Yang and Wilco Nijenhuis and Kapitein, \{Lukas C\} and Florian Berger and Anna Akhmanova",

note = "Funding Information: We thank Lynne Cassimeris (Lehigh University, USA), Pierre G{\"o}nczy and Didier Trono (EPFL, Switzerland), Dr. Duane Compton (Geisel School of Medicine at Dartmouth, USA) and Dr. Laurence Pelletier (Lunenfeld-Tanenbaum Research Institute, Canada) for the gift of materials and Ilya Grigoriev and Eugene Katrukha (Biology Imaging Center, Utrecht University) for the help with imaging and image analysis. This work was supported by China Scholarship Council scholarships to Fangrui Chen, Jingchao Wu and Chao Yang, the Netherlands Organization for Scientific Research Spinoza prize to A.A, as well as the European Research Council Consolidator Grant 819219 to L.C.K. and the Eindhoven-Wageningen-Utrecht Alliance (www.ewuu.nl) that supports the Center for Living Technologies. Funding Information: We?thank?Lynne?Cassimeris?(Lehigh?University,?USA),?Pierre?G{\"o}nczy?and?Didier?Trono?(EPFL,? Switzerland),?Dr.?Duane?Compton?(Geisel?School?of?Medicine?at?Dartmouth,?USA)?and?Dr.?Laurence? Pelletier?(Lunenfeld‐Tanenbaum?Research?Institute,?Canada)?for?the?gift?of?materials?and?Ilya? Grigoriev?and?Eugene?Katrukha?(Biology?Imaging?Center,?Utrecht?University)?for?the?help?with? imaging?and?image?analysis.?This?work?was?supported?by?China?Scholarship?Council?scholarships?to? Fangrui?Chen,?Jingchao?Wu?and?Chao?Yang,?the?Netherlands?Organization?for?Scientific?Research? Spinoza?prize?to?A.A,?as?well?as?the?European?Research?Council?Consolidator?Grant?819219?to?L.C.K.? and?the?Eindhoven‐Wageningen‐Utrecht?Alliance?(www.ewuu.nl)?that?supports?the?Center?for?Living? Technologies.? Publisher Copyright: {\textcopyright} 2022, eLife Sciences Publications Ltd. All rights reserved.",

year = "2022",

month = jul,

day = "5",

doi = "10.7554/eLife.77892",

language = "English",

volume = "11",

pages = "1--47",

journal = "eLife",

issn = "2050-084X",

publisher = "eLife Sciences Publications Ltd",

}

TY - JOUR

T1 - Self-assembly of pericentriolar material in interphase cells lacking centrioles

AU - Chen, Fangrui

AU - Wu, Jingchao

AU - Iwanski, Malina K

AU - Jurriens, Daphne

AU - Sandron, Arianna

AU - Pasolli, Milena

AU - Puma, Gianmarco

AU - Kromhout, Jannes Z

AU - Yang, Chao

AU - Nijenhuis, Wilco

AU - Kapitein, Lukas C

AU - Berger, Florian

AU - Akhmanova, Anna

N1 - Funding Information: We thank Lynne Cassimeris (Lehigh University, USA), Pierre Gönczy and Didier Trono (EPFL, Switzerland), Dr. Duane Compton (Geisel School of Medicine at Dartmouth, USA) and Dr. Laurence Pelletier (Lunenfeld-Tanenbaum Research Institute, Canada) for the gift of materials and Ilya Grigoriev and Eugene Katrukha (Biology Imaging Center, Utrecht University) for the help with imaging and image analysis. This work was supported by China Scholarship Council scholarships to Fangrui Chen, Jingchao Wu and Chao Yang, the Netherlands Organization for Scientific Research Spinoza prize to A.A, as well as the European Research Council Consolidator Grant 819219 to L.C.K. and the Eindhoven-Wageningen-Utrecht Alliance (www.ewuu.nl) that supports the Center for Living Technologies. Funding Information: We?thank?Lynne?Cassimeris?(Lehigh?University,?USA),?Pierre?Gönczy?and?Didier?Trono?(EPFL,? Switzerland),?Dr.?Duane?Compton?(Geisel?School?of?Medicine?at?Dartmouth,?USA)?and?Dr.?Laurence? Pelletier?(Lunenfeld‐Tanenbaum?Research?Institute,?Canada)?for?the?gift?of?materials?and?Ilya? Grigoriev?and?Eugene?Katrukha?(Biology?Imaging?Center,?Utrecht?University)?for?the?help?with? imaging?and?image?analysis.?This?work?was?supported?by?China?Scholarship?Council?scholarships?to? Fangrui?Chen,?Jingchao?Wu?and?Chao?Yang,?the?Netherlands?Organization?for?Scientific?Research? Spinoza?prize?to?A.A,?as?well?as?the?European?Research?Council?Consolidator?Grant?819219?to?L.C.K.? and?the?Eindhoven‐Wageningen‐Utrecht?Alliance?(www.ewuu.nl)?that?supports?the?Center?for?Living? Technologies.? Publisher Copyright: © 2022, eLife Sciences Publications Ltd. All rights reserved.

PY - 2022/7/5

Y1 - 2022/7/5

N2 - The major microtubule-organizing center (MTOC) in animal cells, the centrosome, comprises a pair of centrioles surrounded by pericentriolar material (PCM), which nucleates and anchors microtubules. Centrosome assembly depends on PCM binding to centrioles, PCM self-association and dynein-mediated PCM transport, but the self-assembly properties of PCM components in interphase cells are poorly understood. Here, we used experiments and modeling to study centriole18 independent features of interphase PCM assembly. We showed that when centrioles are lost due to PLK4 depletion or inhibition, dynein-based transport and self-clustering of PCM proteins are sufficient to form a single compact MTOC, which generates a dense radial microtubule array. Interphase self-assembly of PCM components depends on γ-tubulin, pericentrin, CDK5RAP2 and ninein, but not NEDD1, CEP152 or CEP192. Formation of a compact acentriolar MTOC is inhibited by AKAP450-dependent PCM recruitment to the Golgi or by randomly organized CAMSAP2-stabilized microtubules, which keep PCM mobile and prevent its coalescence. Linking of CAMSAP2 to a minus25 end-directed motor leads to the formation of an MTOC, but MTOC compaction requires cooperation with pericentrin-containing self-clustering PCM. Our data reveal that interphase PCM contains a set of components that can self-assemble into a compact structure and organize microtubules, but PCM self-organization is sensitive to motor- and microtubule-based rearrangement.

AB - The major microtubule-organizing center (MTOC) in animal cells, the centrosome, comprises a pair of centrioles surrounded by pericentriolar material (PCM), which nucleates and anchors microtubules. Centrosome assembly depends on PCM binding to centrioles, PCM self-association and dynein-mediated PCM transport, but the self-assembly properties of PCM components in interphase cells are poorly understood. Here, we used experiments and modeling to study centriole18 independent features of interphase PCM assembly. We showed that when centrioles are lost due to PLK4 depletion or inhibition, dynein-based transport and self-clustering of PCM proteins are sufficient to form a single compact MTOC, which generates a dense radial microtubule array. Interphase self-assembly of PCM components depends on γ-tubulin, pericentrin, CDK5RAP2 and ninein, but not NEDD1, CEP152 or CEP192. Formation of a compact acentriolar MTOC is inhibited by AKAP450-dependent PCM recruitment to the Golgi or by randomly organized CAMSAP2-stabilized microtubules, which keep PCM mobile and prevent its coalescence. Linking of CAMSAP2 to a minus25 end-directed motor leads to the formation of an MTOC, but MTOC compaction requires cooperation with pericentrin-containing self-clustering PCM. Our data reveal that interphase PCM contains a set of components that can self-assemble into a compact structure and organize microtubules, but PCM self-organization is sensitive to motor- and microtubule-based rearrangement.

KW - Animals

KW - Centrioles/metabolism

KW - Centrosome/metabolism

KW - Dyneins/metabolism

KW - Interphase

KW - Microtubules/metabolism

KW - Human

KW - PLK4

KW - pericentrin

KW - microtubule-organizing center

KW - pericentriolar material

KW - centrosome

KW - dynein

KW - microtubule

KW - CAMSAP

UR - https://www.scopus.com/pages/publications/85134632306

U2 - 10.7554/eLife.77892

DO - 10.7554/eLife.77892

M3 - Article

C2 - 35787744

SN - 2050-084X

VL - 11

SP - 1

EP - 47

JO - eLife

JF - eLife

M1 - e77892

ER -

Self-assembly of pericentriolar material in interphase cells lacking centrioles

Abstract

Bibliographical note

Keywords

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