ALIX and ESCRT-III Coordinately Control Cytokinetic Abscission During Germline Stem Cell Division in Vivo

Overview

Journal PLoS Genet

Specialty Genetics

Date 2015 Jan 31

PMID 25635693

Citations 23

Authors

Asmund H Eikenes

Lene Malerod

Anette Lie Christensen

Chloe B Steen

Juliette Mathieu

Ioannis P Nezis

Knut Liestol

Jean-Rene Huynh

Harald Stenmark

Kaisa Haglund

Affiliations

Soon will be listed here.

Abstract

Abscission is the final step of cytokinesis that involves the cleavage of the intercellular bridge connecting the two daughter cells. Recent studies have given novel insight into the spatiotemporal regulation and molecular mechanisms controlling abscission in cultured yeast and human cells. The mechanisms of abscission in living metazoan tissues are however not well understood. Here we show that ALIX and the ESCRT-III component Shrub are required for completion of abscission during Drosophila female germline stem cell (fGSC) division. Loss of ALIX or Shrub function in fGSCs leads to delayed abscission and the consequent formation of stem cysts in which chains of daughter cells remain interconnected to the fGSC via midbody rings and fusome. We demonstrate that ALIX and Shrub interact and that they co-localize at midbody rings and midbodies during cytokinetic abscission in fGSCs. Mechanistically, we show that the direct interaction between ALIX and Shrub is required to ensure cytokinesis completion with normal kinetics in fGSCs. We conclude that ALIX and ESCRT-III coordinately control abscission in Drosophila fGSCs and that their complex formation is required for accurate abscission timing in GSCs in vivo.

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References

Neto H, Kaupisch A, Collins L, Gould G . Syntaxin 16 is a master recruitment factor for cytokinesis. Mol Biol Cell. 2013; 24(23):3663-74. PMC: 3842993. DOI: 10.1091/mbc.E13-06-0302. View

Hsu H, LaFever L, Drummond-Barbosa D . Diet controls normal and tumorous germline stem cells via insulin-dependent and -independent mechanisms in Drosophila. Dev Biol. 2007; 313(2):700-12. PMC: 2254938. DOI: 10.1016/j.ydbio.2007.11.006. View

Venken K, Carlson J, Schulze K, Pan H, He Y, Spokony R . Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat Methods. 2009; 6(6):431-4. PMC: 2784134. DOI: 10.1038/nmeth.1331. View

Mathe E, Inoue Y, Palframan W, Brown G, Glover D . Orbit/Mast, the CLASP orthologue of Drosophila, is required for asymmetric stem cell and cystocyte divisions and development of the polarised microtubule network that interconnects oocyte and nurse cells during oogenesis. Development. 2003; 130(5):901-15. DOI: 10.1242/dev.00315. View

Lindas A, Karlsson E, Lindgren M, Ettema T, Bernander R . A unique cell division machinery in the Archaea. Proc Natl Acad Sci U S A. 2008; 105(48):18942-6. PMC: 2596248. DOI: 10.1073/pnas.0809467105. View

Lindas A, Bernander R . The cell cycle of archaea. Nat Rev Microbiol. 2013; 11(9):627-38. DOI: 10.1038/nrmicro3077. View

Wemmer M, Azmi I, West M, Davies B, Katzmann D, Odorizzi G . Bro1 binding to Snf7 regulates ESCRT-III membrane scission activity in yeast. J Cell Biol. 2011; 192(2):295-306. PMC: 3172170. DOI: 10.1083/jcb.201007018. View

McMurray M, Stefan C, Wemmer M, Odorizzi G, Emr S, Thorner J . Genetic interactions with mutations affecting septin assembly reveal ESCRT functions in budding yeast cytokinesis. Biol Chem. 2011; 392(8-9):699-712. PMC: 3381890. DOI: 10.1515/BC.2011.091. View

Huynh J, St Johnston D . The origin of asymmetry: early polarisation of the Drosophila germline cyst and oocyte. Curr Biol. 2004; 14(11):R438-49. DOI: 10.1016/j.cub.2004.05.040. View

10.

Kechad A, Jananji S, Ruella Y, Hickson G . Anillin acts as a bifunctional linker coordinating midbody ring biogenesis during cytokinesis. Curr Biol. 2012; 22(3):197-203. PMC: 3698874. DOI: 10.1016/j.cub.2011.11.062. View

11.

Hudson A, Cooley L . Methods for studying oogenesis. Methods. 2014; 68(1):207-17. PMC: 4048766. DOI: 10.1016/j.ymeth.2014.01.005. View

12.

Iwamori T, Iwamori N, Ma L, Edson M, Greenbaum M, Matzuk M . TEX14 interacts with CEP55 to block cell abscission. Mol Cell Biol. 2010; 30(9):2280-92. PMC: 2863583. DOI: 10.1128/MCB.01392-09. View

13.

Caballe A, Martin-Serrano J . ESCRT machinery and cytokinesis: the road to daughter cell separation. Traffic. 2011; 12(10):1318-26. DOI: 10.1111/j.1600-0854.2011.01244.x. View

14.

Ni J, Zhou R, Czech B, Liu L, Holderbaum L, Yang-Zhou D . A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 2011; 8(5):405-7. PMC: 3489273. DOI: 10.1038/nmeth.1592. View

15.

Fededa J, Gerlich D . Molecular control of animal cell cytokinesis. Nat Cell Biol. 2012; 14(5):440-7. DOI: 10.1038/ncb2482. View

16.

Spradling A, Fuller M, Braun R, Yoshida S . Germline stem cells. Cold Spring Harb Perspect Biol. 2011; 3(11):a002642. PMC: 3220357. DOI: 10.1101/cshperspect.a002642. View

17.

Luo L, Chai P, Cai Y . Immunostaining of germline stem cells and the niche in Drosophila ovaries. Methods Mol Biol. 2013; 1035:1-7. DOI: 10.1007/978-1-62703-508-8_1. View

18.

Barr F, Gruneberg U . Cytokinesis: placing and making the final cut. Cell. 2007; 131(5):847-60. DOI: 10.1016/j.cell.2007.11.011. View

19.

Mondal G, Rowley M, Guidugli L, Wu J, Pankratz V, Couch F . BRCA2 localization to the midbody by filamin A regulates cep55 signaling and completion of cytokinesis. Dev Cell. 2012; 23(1):137-52. PMC: 3419138. DOI: 10.1016/j.devcel.2012.05.008. View

20.

DAvino P, Archambault V, Przewloka M, Zhang W, Laue E, Glover D . Isolation of protein complexes involved in mitosis and cytokinesis from Drosophila cultured cells. Methods Mol Biol. 2009; 545:99-112. DOI: 10.1007/978-1-60327-993-2_6. View