Early Zygotic Gene Product Dunk Interacts with Anillin to Regulate Myosin II During Cleavage

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2023 Jul 26

PMID 37494082

Authors

Jiayang Chen

Andreia F Verissimo

Angela R Kull

Bing He

Affiliations

Soon will be listed here.

Abstract

cellularization is a special form of cleavage that converts syncytial embryos into cellular blastoderms by partitioning the peripherally localized nuclei into individual cells. An early event in cellularization is the recruitment of nonmuscle myosin II ("myosin") to the leading edge of cleavage furrows, where myosin forms an interconnected basal array before reorganizing into individual cytokinetic rings. The initial recruitment and organization of basal myosin are regulated by a cellularization-specific gene, , but the underlying mechanism is unclear. Through a genome-wide yeast two-hybrid screen, we identified anillin (Scraps in ), a conserved scaffolding protein in cytokinesis, as the primary binding partner of Dunk. Dunk colocalizes with anillin and regulates its cortical localization during the formation of cleavage furrows, while the localization of Dunk is independent of anillin. Furthermore, Dunk genetically interacts with anillin to regulate the basal myosin array during cellularization. Similar to Dunk, anillin colocalizes with myosin since the very early stage of cellularization and is required for myosin retention at the basal array, before the well-documented function of anillin in regulating cytokinetic ring assembly. Based on these results, we propose that Dunk regulates myosin recruitment and spatial organization during early cellularization by interacting with and regulating anillin.

References

Mason F, Xie S, Vasquez C, Tworoger M, Martin A . RhoA GTPase inhibition organizes contraction during epithelial morphogenesis. J Cell Biol. 2016; 214(5):603-17. PMC: 5004446. DOI: 10.1083/jcb.201603077. View

Sokac A, Biel N, De Renzis S . Membrane-actin interactions in morphogenesis: Lessons learned from Drosophila cellularization. Semin Cell Dev Biol. 2022; 133:107-122. PMC: 9532467. DOI: 10.1016/j.semcdb.2022.03.028. View

Schweisguth F, Lepesant J, Vincent A . The serendipity alpha gene encodes a membrane-associated protein required for the cellularization of the Drosophila embryo. Genes Dev. 1990; 4(6):922-31. DOI: 10.1101/gad.4.6.922. View

Afshar K, Stuart B, Wasserman S . Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development. 2000; 127(9):1887-97. DOI: 10.1242/dev.127.9.1887. View

Martin A, Kaschube M, Wieschaus E . Pulsed contractions of an actin-myosin network drive apical constriction. Nature. 2008; 457(7228):495-9. PMC: 2822715. DOI: 10.1038/nature07522. View

Pollard T, OShaughnessy B . Molecular Mechanism of Cytokinesis. Annu Rev Biochem. 2019; 88:661-689. PMC: 6588489. DOI: 10.1146/annurev-biochem-062917-012530. View

Rose L, Wieschaus E . The Drosophila cellularization gene nullo produces a blastoderm-specific transcript whose levels respond to the nucleocytoplasmic ratio. Genes Dev. 1992; 6(7):1255-68. DOI: 10.1101/gad.6.7.1255. View

Zhulidov P, Bogdanova E, Shcheglov A, Vagner L, Khaspekov G, Kozhemyako V . Simple cDNA normalization using kamchatka crab duplex-specific nuclease. Nucleic Acids Res. 2004; 32(3):e37. PMC: 373426. DOI: 10.1093/nar/gnh031. View

Field C, Alberts B . Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol. 1995; 131(1):165-78. PMC: 2120607. DOI: 10.1083/jcb.131.1.165. View

10.

Crawford J, Harden N, Leung T, Lim L, Kiehart D . Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function. Dev Biol. 1998; 204(1):151-64. DOI: 10.1006/dbio.1998.9061. View

11.

Zhang L, Wei Y, He Y, Wang X, Huang Z, Sun L . Clinical implication and immunological landscape analyses of ANLN in pan-cancer: A new target for cancer research. Cancer Med. 2022; 12(4):4907-4920. PMC: 9972146. DOI: 10.1002/cam4.5177. View

12.

Budnar S, Husain K, Gomez G, Naghibosadat M, Varma A, Verma S . Anillin Promotes Cell Contractility by Cyclic Resetting of RhoA Residence Kinetics. Dev Cell. 2019; 49(6):894-906.e12. DOI: 10.1016/j.devcel.2019.04.031. View

13.

Grosshans J, Wenzl C, Herz H, Bartoszewski S, Schnorrer F, Vogt N . RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development. 2005; 132(5):1009-20. DOI: 10.1242/dev.01669. View

14.

Yumura S, Ueda M, Sako Y, Kitanishi-Yumura T, Yanagida T . Multiple mechanisms for accumulation of myosin II filaments at the equator during cytokinesis. Traffic. 2008; 9(12):2089-99. DOI: 10.1111/j.1600-0854.2008.00837.x. View

15.

Thomas J, Wieschaus E . src64 and tec29 are required for microfilament contraction during Drosophila cellularization. Development. 2004; 131(4):863-71. DOI: 10.1242/dev.00989. View

16.

Wang D, Chadha G, Feygin A, Ivanov A . F-actin binding protein, anillin, regulates integrity of intercellular junctions in human epithelial cells. Cell Mol Life Sci. 2015; 72(16):3185-3200. PMC: 4506886. DOI: 10.1007/s00018-015-1890-6. View

17.

Sun L, Guan R, Lee I, Liu Y, Chen M, Wang J . Mechanistic insights into the anchorage of the contractile ring by anillin and Mid1. Dev Cell. 2015; 33(4):413-26. PMC: 4449299. DOI: 10.1016/j.devcel.2015.03.003. View

18.

Green R, Paluch E, Oegema K . Cytokinesis in animal cells. Annu Rev Cell Dev Biol. 2012; 28:29-58. DOI: 10.1146/annurev-cellbio-101011-155718. View

19.

Schupbach T, Wieschaus E . Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics. 1989; 121(1):101-17. PMC: 1203592. DOI: 10.1093/genetics/121.1.101. View

20.

Piekny A, Maddox A . The myriad roles of Anillin during cytokinesis. Semin Cell Dev Biol. 2010; 21(9):881-91. DOI: 10.1016/j.semcdb.2010.08.002. View