A membrane reticulum, the centriculum, affects centrosome size and function in Caenorhabditis elegans

Maheshwari, Richa; Rahman, Mohammad Matiur; Drey, Seth; Onyundo, Megan; Fabig, Gunar; Martinez, Michael A Q; Matus, David Q.; Müller‐Reichert, Thomas; Cohen-Fix, Orna

doi:10.1016/j.cub.2022.12.059

Cited by 13 publications

(7 citation statements)

References 81 publications

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“…Then, as the embryos progressed through mitosis, it was progressively excluded from the region between the juxtaposed pronuclei, starting where the characteristic pronuclear membrane scission (gap) event occurs ( Fig. 1C, green arrows ) ( 13 ), and accumulated on the endoplasmic reticulum surrounding the centrosomes, recently named the “centriculum” ( 29 ). By contrast, in lmn-1 8A mutant embryos, where the lamina is not dismantled during mitosis, mCherry::NPP-22 NDC1 also persisted on the juxtaposed pronuclear envelopes ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Mechanisms of Nuclear Pore Complex disassembly by the mitotic Polo-Like Kinase 1 (PLK-1) inC. elegansembryos

Nkoula

Velez-Aguilera

Ossareh-Nazari

et al. 2023

Preprint

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The nuclear envelope, which protects and organizes the interphase genome, is dismantled during mitosis. In the C. elegans zygote, nuclear envelope breakdown (NEBD) of the parental pronuclei is spatially and temporally regulated during mitosis to promote the unification of the parental genomes. During NEBD, Nuclear Pore Complex (NPC) disassembly is critical for rupturing the nuclear permeability barrier and removing the NPCs from the membranes near the centrosomes and between the juxtaposed pronuclei. By combining live imaging, biochemistry, and phosphoproteomics, we characterized NPC disassembly and unveiled the exact role of the mitotic kinase PLK-1 in this process. We show that PLK-1 disassembles the NPC by targeting multiple NPC sub-complexes, including the cytoplasmic filaments, the central channel, and the inner ring. Notably, PLK-1 is recruited to and phosphorylates intrinsically disordered regions of several multivalent linker nucleoporins, a mechanism that appears to be an evolutionarily conserved driver of NPC disassembly during mitosis.

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Section: Resultsmentioning

confidence: 99%

Mechanisms of Nuclear Pore Complex disassembly by the mitotic Polo-Like Kinase 1 (PLK-1) inC. elegansembryos

Nkoula

Velez-Aguilera

Ossareh-Nazari

et al. 2023

Preprint

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“…Thus, the zone of membrane exclusion is nearly equivalent to that of ribosome exclusion in mitosis. Previous reports suggested that mitotic centrosomes are surrounded by an extension of the endoplasmic reticulum termed the ‘centriculum’ (Maheshwari et al, 2023). However, these membranes do not fully enclose the PCM in our data, indicating that the outer boundary of PCM is not entirely defined by membranes; thus, centrosomes should not be considered membrane-enclosed organelles.…”

Section: Resultsmentioning

confidence: 99%

Native molecular architectures of centrosomes inC. elegansembryos

Tollervey,

Rios,

Zagoriy

et al. 2024

Preprint

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Centrosomes organize microtubules that are essential for mitotic divisions in animal cells. They consist of centrioles surrounded by Pericentriolar Material (PCM). Questions related to mechanisms of centriole assembly, PCM organization, and microtubule formation remain unanswered, in part due to limited availability of molecular-resolution structural analyses in situ. Here, we use cryo-electron tomography to visualize centrosomes across the cell cycle in cells isolated from C. elegans embryos. We describe a pseudo-timeline of centriole assembly and identify distinct structural features including a cartwheel in daughter centrioles, and incomplete microtubule doublets surrounded by a star-shaped density in mother centrioles. We find that centriole and PCM microtubules differ in protofilament number (13 versus 11) indicating distinct nucleation mechanisms. This difference could be explained by atypical γ-tubulin ring complexes with 11-fold symmetry identified at the minus ends of short PCM microtubules. We further characterize a porous and disordered network that forms the interconnected PCM. Thus, our work builds a three-dimensional structural atlas that helps explain how centrosomes assemble, grow, and achieve function.

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“…When ER membranes in the vicinity of the spindle poles are exclusively and acutely disrupted in mitotic cells in Drosophila embryos, the spindle becomes smaller, spindle poles detach from the microtubules, and sister chromatid separation velocity slows down [ 47 ]. In C. elegans embryos, ER membranes associated with centrosomes have been shown to regulate microtubule dynamics and spindle function, and potentially assist in NE breakdown [ 50 ]. These data suggest a general function of the ER membranes that are associated with spindle poles in terms of spindle size and function in metazoans.…”

Section: The Mitotic Er: Its Exclusion From Chromosomes Role In Spind...mentioning

confidence: 99%

Sculpting nuclear envelope identity from the endoplasmic reticulum during the cell cycle

Deolal,

Scholz,

Ren

et al. 2024

Nucleus

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The nuclear envelope (NE) regulates nuclear functions, including transcription, nucleocytoplasmic transport, and protein quality control. While the outer membrane of the NE is directly continuous with the endoplasmic reticulum (ER), the NE has an overall distinct protein composition from the ER, which is crucial for its functions. During open mitosis in higher eukaryotes, the NE disassembles during mitotic entry and then reforms as a functional territory at the end of mitosis to reestablish nucleocytoplasmic compartmentalization. In this review, we examine the known mechanisms by which the functional NE reconstitutes from the mitotic ER in the continuous ER–NE endomembrane system during open mitosis. Furthermore, based on recent findings indicating that the NE possesses unique lipid metabolism and quality control mechanisms distinct from those of the ER, we explore the maintenance of NE identity and homeostasis during interphase. We also highlight the potential significance of membrane junctions between the ER and NE.

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A membrane reticulum, the centriculum, affects centrosome size and function in Caenorhabditis elegans

Cited by 13 publications

References 81 publications

Mechanisms of Nuclear Pore Complex disassembly by the mitotic Polo-Like Kinase 1 (PLK-1) inC. elegansembryos

Mechanisms of Nuclear Pore Complex disassembly by the mitotic Polo-Like Kinase 1 (PLK-1) inC. elegansembryos

Native molecular architectures of centrosomes inC. elegansembryos

Sculpting nuclear envelope identity from the endoplasmic reticulum during the cell cycle

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