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Cytoskeletal Dynamics and Regulation of Cell Cycle Progression

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Biochemistry".

Deadline for manuscript submissions: closed (30 April 2022) | Viewed by 14021

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Special Issue Editors

Prof. Dr. Leah Gheber

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Guest Editor

Ilse Katz Inst Nanoscale Sci & Technol, Ben-Gurion University of the Negev, IL-84105 Beer Sheva, Israel
Interests: mitotic-spindle; kinesin-related motor proteins; cell-cycle; cancer; microtubule; cytoskeleton

Prof. Dr. Mart Loog

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Guest Editor

University of Tartudisabled, Tartu, Estonia

Special Issue Information

Dear Colleagues,

The correct transmission of genetic information from one generation to the next and the successful completion of mitosis depend on the temporal and spatial coordination of many mitotic processes such as mitotic spindle assembly, chromosome segregation and spindle elongation, spindle disassembly, and cytokinesis. To ensure correct chromosome segregation, spindle morphogenesis and cell cycle progression are monitored by multiple surveillance systems that include a number of protein kinases and phosphatases controlling and affecting the phosphorylation of mitotic proteins, thus regulating their activity and intracellular localization.

Morphological changes of the mitotic spindle are governed, in part, by the dynamics of cytoskeletal filaments—actin filaments and microtubules—and by the functions of molecular motors of the myosin, dynein, and kinesin superfamilies, which utilize energy from ATP hydrolysis to produce nanometric directional steps along the filaments of the cytoskeleton. The regulation and coordination of cytoskeletal dynamics and of molecular motors is of critical importance to correctly segregate chromosomes and allow cell cycle progression. Despite major research efforts during the last decades, the mechanisms by which cytoskeletal dynamics is controlled and coordinated by the cell cycle surveillance machinery remain elusive.

In recent years, new advances in microscopic imaging and biophysical and biochemical techniques, as well as advances in cryo-electron microscopy have led to scientific breakthroughs allowing a new understanding of the regulation mechanisms and cytoskeletal dynamics during cell cycle progression. In this Special Issue, we will highlight the recent advances in this field and discuss open questions and future directions.

Prof. Dr. Leah Gheber
Prof. Dr. Mart Loog
Guest Editors

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Keywords

kinesin
dynein
myosin
mitosis, cell cycle
kinases, phosphatases, microtubules
actin filaments
intracellular trafficking

Published Papers (5 papers)

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Research

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16 pages, 3253 KiB

Open AccessArticle

Docking to a Basic Helix Promotes Specific Phosphorylation by G1-Cdk1

by Ilona Faustova, Kaidi Möll, Ervin Valk, Mart Loog and Mihkel Örd

Int. J. Mol. Sci. 2021, 22(17), 9514; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22179514 - 01 Sep 2021

Cited by 2 | Viewed by 2247

Abstract

Cyclins are the activators of cyclin-dependent kinase (CDK) complex, but they also act as docking scaffolds for different short linear motifs (SLiMs) in CDK substrates and inhibitors. According to the unified model of CDK function, the cell cycle is coordinated by CDK both via general CDK activity thresholds and cyclin-specific substrate docking. Recently, it was found that the G1-cyclins of S. cerevisiae have a specific function in promoting polarization and growth of the buds, making the G1 cyclins essential for cell survival. Thus, while a uniform CDK specificity of a single cyclin can be sufficient to drive the cell cycle in some cells, such as in fission yeast, cyclin specificity can be essential in other organisms. However, the known G1-CDK specific LP docking motif, was not responsible for this essential function, indicating that G1-CDKs use yet other unknown docking mechanisms. Here we report a discovery of a G1 cyclin-specific (Cln1,2) lysine-arginine-rich helical docking motif (the K/R motif) in G1-CDK targets involved in the mating pathway (Ste7), transcription (Xbp1), bud morphogenesis (Bud2) and spindle pole body (Spc29, Spc42, Spc110, Sli15) function of S. cerevisiae. We also show that the docking efficiency of K/R motif can be regulated by basophilic kinases such as protein kinase A. Our results further widen the list of cyclin specificity mechanisms and may explain the recently demonstrated unique essential function of G1 cyclins in budding yeast. Full article

(This article belongs to the Special Issue Cytoskeletal Dynamics and Regulation of Cell Cycle Progression)

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31 pages, 4257 KiB

Open AccessArticle

Nano-Particles Carried by Multiple Dynein Motors Self-Regulate Their Number of Actively Participating Motors

by Gal Halbi, Itay Fayer, Dina Aranovich, Shachar Gat, Shay Bar, Vitaly Erukhimovitch, Rony Granek and Anne Bernheim-Groswasser

Int. J. Mol. Sci. 2021, 22(16), 8893; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168893 - 18 Aug 2021

Cited by 3 | Viewed by 2086

Abstract

Intra-cellular active transport by native cargos is ubiquitous. We investigate the motion of spherical nano-particles (NPs) grafted with flexible polymers that end with a nuclear localization signal peptide. This peptide allows the recruitment of several mammalian dynein motors from cytoplasmic extracts. To determine how motor–motor interactions influenced motility on the single microtubule level, we conducted bead-motility assays incorporating surface adsorbed microtubules and combined them with model simulations that were based on the properties of a single dynein. The experimental and simulation results revealed long time trajectories: when the number of NP-ligated motors N_m increased, run-times and run-lengths were enhanced and mean velocities were somewhat decreased. Moreover, the dependence of the velocity on run-time followed a universal curve, regardless of the system composition. Model simulations also demonstrated left- and right-handed helical motion and revealed self-regulation of the number of microtubule-bound, actively transporting dynein motors. This number was stochastic along trajectories and was distributed mainly between one, two, and three motors, regardless of N_m. We propose that this self-regulation allows our synthetic NPs to achieve persistent motion that is associated with major helicity. Such a helical motion might affect obstacle bypassing, which can influence active transport efficiency when facing the crowded environment of the cell. Full article

(This article belongs to the Special Issue Cytoskeletal Dynamics and Regulation of Cell Cycle Progression)

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18 pages, 1894 KiB

Open AccessArticle

Effect of Kinesin-5 Tail Domain on Motor Dynamics for Antiparallel Microtubule Sliding

by Yuying Liu, Yao Wang, Pengye Wang and Ping Xie

Int. J. Mol. Sci. 2021, 22(15), 7857; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22157857 - 23 Jul 2021

Cited by 4 | Viewed by 1400

Abstract

Kinesin-5 motor consists of two pairs of heads and tail domains, which are situated at the opposite ends of a common stalk. The two pairs of heads can bind to two antiparallel microtubules (MTs) and move on the two MTs independently towards the plus ends, sliding apart the two MTs, which is responsible for chromosome segregation during mitosis. Prior experimental data showed that the tails of kinesin-5 Eg5 can modulate the dynamics of single motors and are critical for multiple motors to generate high steady forces to slide apart two antiparallel MTs. To understand the molecular mechanism of the tails modulating the ability of Eg5 motors, based on our proposed model the dynamics of the single Eg5 with the tails and that without the tails moving on single MTs is studied analytically and compared. Furthermore, the dynamics of antiparallel MT sliding by multiple Eg5 motors with the tails and that without the tails is studied numerically and compared. Both the analytical results for single motors and the numerical results for multiple motors are consistent with the available experimental data. Full article

(This article belongs to the Special Issue Cytoskeletal Dynamics and Regulation of Cell Cycle Progression)

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17 pages, 5161 KiB

Open AccessArticle

The Putative RNA-Binding Protein Dri1 Promotes the Loading of Kinesin-14/Klp2 to the Mitotic Spindle and Is Sequestered into Heat-Induced Protein Aggregates in Fission Yeast

by Masashi Yukawa, Mitsuki Ohishi, Yusuke Yamada and Takashi Toda

Int. J. Mol. Sci. 2021, 22(9), 4795; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22094795 - 30 Apr 2021

Cited by 2 | Viewed by 2502

Abstract

Cells form a bipolar spindle during mitosis to ensure accurate chromosome segregation. Proper spindle architecture is established by a set of kinesin motors and microtubule-associated proteins. In most eukaryotes, kinesin-5 motors are essential for this process, and genetic or chemical inhibition of their activity leads to the emergence of monopolar spindles and cell death. However, these deficiencies can be rescued by simultaneous inactivation of kinesin-14 motors, as they counteract kinesin-5. We conducted detailed genetic analyses in fission yeast to understand the mechanisms driving spindle assembly in the absence of kinesin-5. Here, we show that deletion of the dri1 gene, which encodes a putative RNA-binding protein, can rescue temperature sensitivity caused by cut7-22, a fission yeast kinesin-5 mutant. Interestingly, kinesin-14/Klp2 levels on the spindles in the cut7 mutants were significantly reduced by the dri1 deletion, although the total levels of Klp2 and the stability of spindle microtubules remained unaffected. Moreover, RNA-binding motifs of Dri1 are essential for its cytoplasmic localization and function. We have also found that a portion of Dri1 is spatially and functionally sequestered by chaperone-based protein aggregates upon mild heat stress and limits cell division at high temperatures. We propose that Dri1 might be involved in post-transcriptional regulation through its RNA-binding ability to promote the loading of Klp2 on the spindle microtubules. Full article

(This article belongs to the Special Issue Cytoskeletal Dynamics and Regulation of Cell Cycle Progression)

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Review

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25 pages, 3593 KiB

Open AccessReview

Mechanisms by Which Kinesin-5 Motors Perform Their Multiple Intracellular Functions

by Himanshu Pandey, Mary Popov, Alina Goldstein-Levitin and Larisa Gheber

Int. J. Mol. Sci. 2021, 22(12), 6420; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22126420 - 15 Jun 2021

Cited by 7 | Viewed by 4346

Abstract

Bipolar kinesin-5 motor proteins perform multiple intracellular functions, mainly during mitotic cell division. Their specialized structural characteristics enable these motors to perform their essential functions by crosslinking and sliding apart antiparallel microtubules (MTs). In this review, we discuss the specialized structural features of kinesin-5 motors, and the mechanisms by which these features relate to kinesin-5 functions and motile properties. In addition, we discuss the multiple roles of the kinesin-5 motors in dividing as well as in non-dividing cells, and examine their roles in pathogenetic conditions. We describe the recently discovered bidirectional motility in fungi kinesin-5 motors, and discuss its possible physiological relevance. Finally, we also focus on the multiple mechanisms of regulation of these unique motor proteins. Full article

(This article belongs to the Special Issue Cytoskeletal Dynamics and Regulation of Cell Cycle Progression)

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