Moesin is Involved in Polarity Maintenance and Cortical Remodeling During Asymmetric Cell Division

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2017 Dec 29

PMID 29282284

Citations 9

Authors

Namal Abeysundara

Andrew J Simmonds

Sarah C Hughes

Affiliations

Soon will be listed here.

Abstract

An intact actomyosin network is essential for anchoring polarity proteins to the cell cortex and maintaining cell size asymmetry during asymmetric cell division of neuroblasts (NBs). However, the mechanisms that control changes in actomyosin dynamics during asymmetric cell division remain unclear. We find that the actin-binding protein, Moesin, is essential for NB proliferation and mitotic progression in the developing brain. During metaphase, phosphorylated Moesin (p-Moesin) is enriched at the apical cortex, and loss of Moesin leads to defects in apical polarity maintenance and cortical stability. This asymmetric distribution of p-Moesin is determined by components of the apical polarity complex and Slik kinase. During later stages of mitosis, p-Moesin localization shifts more basally, contributing to asymmetric cortical extension and myosin basal furrow positioning. Our findings reveal Moesin as a novel apical polarity protein that drives cortical remodeling of dividing NBs, which is essential for polarity maintenance and initial establishment of cell size asymmetry.

Citing Articles

The Drosophila neuroblast polarity cycle at a glance.

Penkert R, LaFoya B, Moholt-Siebert L, Vargas E, Welch S, Prehoda K J Cell Sci. 2024; 137(5).

PMID: 38465513 PMC: 10984279. DOI: 10.1242/jcs.261789.

Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies.

Cicconardi F, Milanetti E, Pinheiro de Castro E, Mazo-Vargas A, Van Belleghem S, Ruggieri A Nat Commun. 2023; 14(1):5620.

PMID: 37699868 PMC: 10497600. DOI: 10.1038/s41467-023-41412-5.

Alzheimer's disease and related tauopathies: disorders of disrupted neuronal identity.

Frost B Trends Neurosci. 2023; 46(10):797-813.

PMID: 37591720 PMC: 10528597. DOI: 10.1016/j.tins.2023.07.006.

A chromatin remodelling SWI/SNF subunit, Snr1, regulates neural stem cell determination and differentiation.

Keegan S, Haskins J, Simmonds A, Hughes S Development. 2023; 150(13).

PMID: 37294080 PMC: 10323235. DOI: 10.1242/dev.201484.

A biophysical perspective of the regulatory mechanisms of ezrin/radixin/moesin proteins.

Senju Y, Tsai F Biophys Rev. 2022; 14(1):199-208.

PMID: 35340609 PMC: 8921360. DOI: 10.1007/s12551-021-00928-0.

References

Verboon J, Parkhurst S . Rho family GTPases bring a familiar ring to cell wound repair. Small GTPases. 2015; 6(1):1-7. PMC: 4601322. DOI: 10.4161/21541248.2014.992262. View

Luxenburg C, Pasolli H, Williams S, Fuchs E . Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat Cell Biol. 2011; 13(3):203-14. PMC: 3278337. DOI: 10.1038/ncb2163. View

Lu B, Ackerman L, Jan L, Jan Y . Modes of protein movement that lead to the asymmetric localization of partner of Numb during Drosophila neuroblast division. Mol Cell. 2000; 4(6):883-91. DOI: 10.1016/s1097-2765(00)80218-x. View

Wodarz A, Ramrath A, Kuchinke U, Knust E . Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature. 1999; 402(6761):544-7. DOI: 10.1038/990128. View

Bowman S, Neumuller R, Novatchkova M, Du Q, Knoblich J . The Drosophila NuMA Homolog Mud regulates spindle orientation in asymmetric cell division. Dev Cell. 2006; 10(6):731-42. DOI: 10.1016/j.devcel.2006.05.005. View

Thery M, Racine V, Pepin A, Piel M, Chen Y, Sibarita J . The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol. 2005; 7(10):947-53. DOI: 10.1038/ncb1307. View

Gobel V, Barrett P, Hall D, Fleming J . Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev Cell. 2004; 6(6):865-73. DOI: 10.1016/j.devcel.2004.05.018. View

White K, Grether M, Abrams J, Young L, Farrell K, Steller H . Genetic control of programmed cell death in Drosophila. Science. 1994; 264(5159):677-83. DOI: 10.1126/science.8171319. View

Hayashi K, Yonemura S, Matsui T, Tsukita S . Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues. J Cell Sci. 1999; 112 ( Pt 8):1149-58. DOI: 10.1242/jcs.112.8.1149. View

10.

Kunda P, Rodrigues N, Moeendarbary E, Liu T, Ivetic A, Charras G . PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Curr Biol. 2012; 22(3):231-6. DOI: 10.1016/j.cub.2011.12.016. View

11.

Lerit D, Plevock K, Rusan N . Live imaging of Drosophila larval neuroblasts. J Vis Exp. 2014; (89). PMC: 4129452. DOI: 10.3791/51756. View

12.

Barros C, Phelps C, Brand A . Drosophila nonmuscle myosin II promotes the asymmetric segregation of cell fate determinants by cortical exclusion rather than active transport. Dev Cell. 2003; 5(6):829-40. DOI: 10.1016/s1534-5807(03)00359-9. View

13.

Wodarz A, Ramrath A, Grimm A, Knust E . Drosophila atypical protein kinase C associates with Bazooka and controls polarity of epithelia and neuroblasts. J Cell Biol. 2000; 150(6):1361-74. PMC: 2150710. DOI: 10.1083/jcb.150.6.1361. View

14.

Turunen O, Wahlstrom T, Vaheri A . Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J Cell Biol. 1994; 126(6):1445-53. PMC: 2290954. DOI: 10.1083/jcb.126.6.1445. View

15.

Sabino D, Gogendeau D, Gambarotto D, Nano M, Pennetier C, Dingli F . Moesin is a major regulator of centrosome behavior in epithelial cells with extra centrosomes. Curr Biol. 2015; 25(7):879-89. PMC: 4386030. DOI: 10.1016/j.cub.2015.01.066. View

16.

Ito K, Hotta Y . Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol. 1992; 149(1):134-48. DOI: 10.1016/0012-1606(92)90270-q. View

17.

Ding R, Weynans K, Bossing T, Barros C, Berger C . The Hippo signalling pathway maintains quiescence in Drosophila neural stem cells. Nat Commun. 2016; 7:10510. PMC: 4740179. DOI: 10.1038/ncomms10510. View

18.

Jiang Y, Reichert H . Drosophila neural stem cells in brain development and tumor formation. J Neurogenet. 2014; 28(3-4):181-9. DOI: 10.3109/01677063.2014.898639. View

19.

Algrain M, Turunen O, Vaheri A, Louvard D, Arpin M . Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker. J Cell Biol. 1993; 120(1):129-39. PMC: 2119498. DOI: 10.1083/jcb.120.1.129. View

20.

Berryman M, Franck Z, BRETSCHER A . Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cells whereas moesin is found primarily in endothelial cells. J Cell Sci. 1993; 105 ( Pt 4):1025-43. DOI: 10.1242/jcs.105.4.1025. View