Roles of ESCRT-III Polymers in Cell Division Across the Tree of Life

Overview

Journal Curr Opin Cell Biol

Publisher Elsevier

Specialty Cell Biology

Date 2023 Nov 9

PMID 37944425

Authors

Jeremy Graham Carlton

Buzz Baum

Affiliations

Soon will be listed here.

Abstract

Every cell becomes two through a carefully orchestrated process of division. Prior to division, contractile machinery must first be assembled at the cell midzone to ensure that the cut, when it is made, bisects the two separated copies of the genetic material. Second, this contractile machinery must be dynamically tethered to the limiting plasma membrane so as to bring the membrane with it as it constricts. Finally, the connecting membrane must be severed to generate two physically separate daughter cells. In several organisms across the tree of life, Endosomal Sorting Complex Required for Transport (ESCRT)-III family proteins aid cell division by forming composite polymers that function together with the Vps4 AAA-ATPase to constrict and cut the membrane tube connecting nascent daughter cells from the inside. In this review, we discuss unique features of ESCRT-III that enable it to play this role in division in many archaea and eukaryotes.

Citing Articles

Asgard archaea reveal the conserved principles of ESCRT-III membrane remodeling.

Souza D, Espadas J, Chaaban S, Moody E, Hatano T, Balasubramanian M Sci Adv. 2025; 11(6):eads5255.

PMID: 39919172 PMC: 11804906. DOI: 10.1126/sciadv.ads5255.

A relay race of ESCRT-III paralogs drives cell division in a hyperthermophilic archaeon.

Liu J, Lelek M, Yang Y, Salles A, Zimmer C, Shen Y mBio. 2024; 16(2):e0099124.

PMID: 39699168 PMC: 11796394. DOI: 10.1128/mbio.00991-24.

Monomer unfolding of a bacterial ESCRT-III superfamily member is coupled to oligomer disassembly.

Quarta N, Bhandari T, Girard M, Hellmann N, Schneider D Protein Sci. 2024; 33(11):e5187.

PMID: 39470325 PMC: 11520248. DOI: 10.1002/pro.5187.

Structural basis for Vipp1 membrane binding: from loose coats and carpets to ring and rod assemblies.

Junglas B, Kartte D, Kutzner M, Hellmann N, Ritter I, Schneider D Nat Struct Mol Biol. 2024; .

PMID: 39379528 DOI: 10.1038/s41594-024-01399-z.

HRS Facilitates Newcastle Disease Virus Replication in Tumor Cells by Promoting Viral Budding.

Chen Y, Wang C, Hu S, Liu X Int J Mol Sci. 2024; 25(18).

PMID: 39337546 PMC: 11432301. DOI: 10.3390/ijms251810060.

References

McCullough J, Clippinger A, Talledge N, Skowyra M, Saunders M, Naismith T . Structure and membrane remodeling activity of ESCRT-III helical polymers. Science. 2015; 350(6267):1548-51. PMC: 4684769. DOI: 10.1126/science.aad8305. View

Atilla-Gokcumen G, Muro E, Relat-Goberna J, Sasse S, Bedigian A, Coughlin M . Dividing cells regulate their lipid composition and localization. Cell. 2014; 156(3):428-39. PMC: 3909459. DOI: 10.1016/j.cell.2013.12.015. View

Chiaruttini N, Redondo-Morata L, Colom A, Humbert F, Lenz M, Scheuring S . Relaxation of Loaded ESCRT-III Spiral Springs Drives Membrane Deformation. Cell. 2015; 163(4):866-79. PMC: 4644223. DOI: 10.1016/j.cell.2015.10.017. View

Ellen A, Albers S, Huibers W, Pitcher A, Hobel C, Schwarz H . Proteomic analysis of secreted membrane vesicles of archaeal Sulfolobus species reveals the presence of endosome sorting complex components. Extremophiles. 2008; 13(1):67-79. DOI: 10.1007/s00792-008-0199-x. View

Adell M, Migliano S, Upadhyayula S, Bykov Y, Sprenger S, Pakdel M . Recruitment dynamics of ESCRT-III and Vps4 to endosomes and implications for reverse membrane budding. Elife. 2017; 6. PMC: 5665648. DOI: 10.7554/eLife.31652. View

Arimura S, Tsutsumi N . A dynamin-like protein (ADL2b), rather than FtsZ, is involved in Arabidopsis mitochondrial division. Proc Natl Acad Sci U S A. 2002; 99(8):5727-31. PMC: 122839. DOI: 10.1073/pnas.082663299. View

Bernander R . The cell cycle of Sulfolobus. Mol Microbiol. 2007; 66(3):557-62. DOI: 10.1111/j.1365-2958.2007.05917.x. View

Lancaster O, Le Berre M, Dimitracopoulos A, Bonazzi D, Zlotek-Zlotkiewicz E, Picone R . Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. Dev Cell. 2013; 25(3):270-83. DOI: 10.1016/j.devcel.2013.03.014. View

Denais C, Gilbert R, Isermann P, McGregor A, Te Lindert M, Weigelin B . Nuclear envelope rupture and repair during cancer cell migration. Science. 2016; 352(6283):353-8. PMC: 4833568. DOI: 10.1126/science.aad7297. View

10.

Gupta T, Klumpe S, Gries K, Heinz S, Wietrzynski W, Ohnishi N . Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity. Cell. 2021; 184(14):3643-3659.e23. DOI: 10.1016/j.cell.2021.05.011. View

11.

Takahashi Y, He H, Tang Z, Hattori T, Liu Y, Young M . An autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure. Nat Commun. 2018; 9(1):2855. PMC: 6054611. DOI: 10.1038/s41467-018-05254-w. View

12.

Szwedziak P, Wang Q, Bharat T, Tsim M, Lowe J . Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. Elife. 2014; 3:e04601. PMC: 4383033. DOI: 10.7554/eLife.04601. View

13.

Carlton J, Caballe A, Agromayor M, Kloc M, Martin-Serrano J . ESCRT-III governs the Aurora B-mediated abscission checkpoint through CHMP4C. Science. 2012; 336(6078):220-5. PMC: 3998087. DOI: 10.1126/science.1217180. View

14.

Soderstrom B, Skoog K, Blom H, Weiss D, von Heijne G, Daley D . Disassembly of the divisome in Escherichia coli: evidence that FtsZ dissociates before compartmentalization. Mol Microbiol. 2014; 92(1):1-9. PMC: 4004784. DOI: 10.1111/mmi.12534. View

15.

Krupka M, Margolin W . Unite to divide: Oligomerization of tubulin and actin homologs regulates initiation of bacterial cell division. F1000Res. 2018; 7:235. PMC: 5832921. DOI: 10.12688/f1000research.13504.1. View

16.

Olmos Y, Perdrix-Rosell A, Carlton J . Membrane Binding by CHMP7 Coordinates ESCRT-III-Dependent Nuclear Envelope Reformation. Curr Biol. 2016; 26(19):2635-2641. PMC: 5069351. DOI: 10.1016/j.cub.2016.07.039. View

17.

Christ L, Wenzel E, Liestol K, Raiborg C, Campsteijn C, Stenmark H . ALIX and ESCRT-I/II function as parallel ESCRT-III recruiters in cytokinetic abscission. J Cell Biol. 2016; 212(5):499-513. PMC: 4772496. DOI: 10.1083/jcb.201507009. View

18.

Samson R, Obita T, Hodgson B, Shaw M, Chong P, Williams R . Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol Cell. 2011; 41(2):186-96. PMC: 3763469. DOI: 10.1016/j.molcel.2010.12.018. View

19.

Liu J, Tassinari M, Souza D, Naskar S, Noel J, Bohuszewicz O . Bacterial Vipp1 and PspA are members of the ancient ESCRT-III membrane-remodeling superfamily. Cell. 2021; 184(14):3660-3673.e18. PMC: 8281802. DOI: 10.1016/j.cell.2021.05.041. View

20.

Wenzel D, Mackay D, Skalicky J, Paine E, Miller M, Ullman K . Comprehensive analysis of the human ESCRT-III-MIT domain interactome reveals new cofactors for cytokinetic abscission. Elife. 2022; 11. PMC: 9477494. DOI: 10.7554/eLife.77779. View