Microtubules Move the Nucleus to Quiescence

Overview

Journal Nucleus

Date 2014 Mar 19

PMID 24637834

Citations 8

Authors

Damien Laporte

Isabelle Sagot

Affiliations

Soon will be listed here.

Abstract

The nucleus is a cellular compartment that hosts several macro-molecular machines displaying a highly complex spatial organization. This tight architectural orchestration determines not only DNA replication and repair but also regulates gene expression. In budding yeast microtubules play a key role in structuring the nucleus since they condition the Rabl arrangement in G1 and chromosome partitioning during mitosis through their attachment to centromeres via the kinetochore proteins. Recently, we have shown that upon quiescence entry, intranuclear microtubules emanating from the spindle pole body elongate to form a highly stable bundle that spans the entire nucleus. Here, we examine some molecular mechanisms that may underlie the formation of this structure. As the intranuclear microtubule bundle causes a profound re-organization of the yeast nucleus and is required for cell survival during quiescence, we discuss the possibility that the assembly of such a structure participates in quiescence establishment.

Citing Articles

A stable microtubule bundle formed through an orchestrated multistep process controls quiescence exit.

Laporte D, Massoni-Laporte A, Lefranc C, Dompierre J, Mauboules D, Nsamba E Elife. 2024; 12.

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Chromatin Dynamics During Entry to Quiescence and Compromised Functionality in Cancer Cells.

Dobbs O, Coverley D Results Probl Cell Differ. 2022; 70:279-294.

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Moonlighting at the Poles: Non-Canonical Functions of Centrosomes.

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Mechanisms that Link Chronological Aging to Cellular Quiescence in Budding Yeast.

Mohammad K, Junio J, Tafakori T, Orfanos E, Titorenko V Int J Mol Sci. 2020; 21(13).

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Nuclear envelope attachment of telomeres limits TERRA and telomeric rearrangements in quiescent fission yeast cells.

Maestroni L, Reyes C, Vaurs M, Gachet Y, Tournier S, Geli V Nucleic Acids Res. 2020; 48(6):3029-3041.

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References

Kitamura E, Tanaka K, Kitamura Y, Tanaka T . Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. Genes Dev. 2007; 21(24):3319-30. PMC: 2113032. DOI: 10.1101/gad.449407. View

Kim S, Tsiokas L . Cilia and cell cycle re-entry: more than a coincidence. Cell Cycle. 2011; 10(16):2683-90. PMC: 3219538. DOI: 10.4161/cc.10.16.17009. View

YOTSUYANAGI Y . [Study of yeast mitochondria. I. Variations in mitochondrial ultrastructure during the aerobic growth cycle]. J Ultrastruct Res. 1962; 7:121-40. DOI: 10.1016/s0022-5320(62)80031-8. View

Miranda J, De Wulf P, Sorger P, Harrison S . The yeast DASH complex forms closed rings on microtubules. Nat Struct Mol Biol. 2005; 12(2):138-43. DOI: 10.1038/nsmb896. View

Hunt A, McIntosh J . The dynamic behavior of individual microtubules associated with chromosomes in vitro. Mol Biol Cell. 1998; 9(10):2857-71. PMC: 25560. DOI: 10.1091/mbc.9.10.2857. View

Laporte D, Lebaudy A, Sahin A, Pinson B, Ceschin J, Daignan-Fornier B . Metabolic status rather than cell cycle signals control quiescence entry and exit. J Cell Biol. 2011; 192(6):949-57. PMC: 3063145. DOI: 10.1083/jcb.201009028. View

Laporte D, Salin B, Daignan-Fornier B, Sagot I . Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol. 2008; 181(5):737-45. PMC: 2396804. DOI: 10.1083/jcb.200711154. View

Wells A, Griffith L, Wells J, Taylor D . The dormancy dilemma: quiescence versus balanced proliferation. Cancer Res. 2013; 73(13):3811-6. PMC: 3702639. DOI: 10.1158/0008-5472.CAN-13-0356. View

Jensen P, Larsson L . Actin microdomains on endothelial cells: association with CD44, ERM proteins, and signaling molecules during quiescence and wound healing. Histochem Cell Biol. 2004; 121(5):361-9. DOI: 10.1007/s00418-004-0648-2. View

10.

Cooper S . Reappraisal of serum starvation, the restriction point, G0, and G1 phase arrest points. FASEB J. 2003; 17(3):333-40. DOI: 10.1096/fj.02-0352rev. View

11.

Martinez M, Roy S, Archuletta A, Wentzell P, Anna-Arriola S, Rodriguez A . Genomic analysis of stationary-phase and exit in Saccharomyces cerevisiae: gene expression and identification of novel essential genes. Mol Biol Cell. 2004; 15(12):5295-305. PMC: 532011. DOI: 10.1091/mbc.e03-11-0856. View

12.

Jin Q, Trelles-Sticken E, Scherthan H, Loidl J . Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol. 1998; 141(1):21-9. PMC: 2132713. DOI: 10.1083/jcb.141.1.21. View

13.

Sagot I, Pinson B, Salin B, Daignan-Fornier B . Actin bodies in yeast quiescent cells: an immediately available actin reserve?. Mol Biol Cell. 2006; 17(11):4645-55. PMC: 1635378. DOI: 10.1091/mbc.e06-04-0282. View

14.

Coller H, Sang L, Roberts J . A new description of cellular quiescence. PLoS Biol. 2006; 4(3):e83. PMC: 1393757. DOI: 10.1371/journal.pbio.0040083. View

15.

Blake-Hodek K, Cassimeris L, Huffaker T . Regulation of microtubule dynamics by Bim1 and Bik1, the budding yeast members of the EB1 and CLIP-170 families of plus-end tracking proteins. Mol Biol Cell. 2010; 21(12):2013-23. PMC: 2883945. DOI: 10.1091/mbc.e10-02-0083. View

16.

Radonjic M, Andrau J, Lijnzaad P, Kemmeren P, Kockelkorn T, van Leenen D . Genome-wide analyses reveal RNA polymerase II located upstream of genes poised for rapid response upon S. cerevisiae stationary phase exit. Mol Cell. 2005; 18(2):171-83. DOI: 10.1016/j.molcel.2005.03.010. View

17.

Howard J, Hyman A . Microtubule polymerases and depolymerases. Curr Opin Cell Biol. 2006; 19(1):31-5. DOI: 10.1016/j.ceb.2006.12.009. View

18.

Liu I, Chiu S, Lee H, Leu J . The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells. Mol Biol Cell. 2012; 23(7):1231-42. PMC: 3315813. DOI: 10.1091/mbc.E11-09-0752. View

19.

OToole E, Winey M, McIntosh J . High-voltage electron tomography of spindle pole bodies and early mitotic spindles in the yeast Saccharomyces cerevisiae. Mol Biol Cell. 1999; 10(6):2017-31. PMC: 25406. DOI: 10.1091/mbc.10.6.2017. View

20.

Narayanaswamy R, Levy M, Tsechansky M, Stovall G, OConnell J, Mirrielees J . Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc Natl Acad Sci U S A. 2009; 106(25):10147-52. PMC: 2691686. DOI: 10.1073/pnas.0812771106. View