Title: Actomyosin Tube Formation in Polar Body Cytokinesis Requires Anillin in C. elegans
Abstract: Polar body extrusion (PBE) is the specialized asymmetric division by which oocytes accomplish reduction in ploidy and retention of cytoplasm. During maternal gametogenesis, as in male meiosis and mitosis, cytokinesis is accomplished by a ring rich in active Rho, myosin, and formin-nucleated F-actin [1Deng M. Suraneni P. Schultz R.M. Li R. The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes.Dev. Cell. 2007; 12: 301-308Abstract Full Text Full Text PDF PubMed Scopus (136) Google Scholar, 2Dumont J. Million K. Sunderland K. Rassinier P. Lim H. Leader B. Verlhac M.H. Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes.Dev. Biol. 2007; 301: 254-265Crossref PubMed Scopus (141) Google Scholar, 3Longo F.J. The effects of cytochalasin B on the events of fertilization in the surf clam, Spisula solidissima. I. Polar body formation.J. Exp. Zool. 1972; 182: 321-344Crossref PubMed Scopus (57) Google Scholar, 4Ma C. Benink H.A. Cheng D. Montplaisir V. Wang L. Xi Y. Zheng P.P. Bement W.M. Liu X.J. Cdc42 activation couples spindle positioning to first polar body formation in oocyte maturation.Curr. Biol. 2006; 16: 214-220Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar, 5Moore G.D. Ayabe T. Visconti P.E. Schultz R.M. Kopf G.S. Roles of heterotrimeric and monomeric G proteins in sperm-induced activation of mouse eggs.Development. 1994; 120: 3313-3323Crossref PubMed Google Scholar, 6Zhang X. Ma C. Miller A.L. Katbi H.A. Bement W.M. Liu X.J. Polar body emission requires a RhoA contractile ring and Cdc42-mediated membrane protrusion.Dev. Cell. 2008; 15: 386-400Abstract Full Text Full Text PDF PubMed Scopus (60) Google Scholar, 7Zhong Z.S. Huo L.J. Liang C.G. Chen D.Y. Sun Q.Y. Small GTPase RhoA is required for ooplasmic segregation and spindle rotation, but not for spindle organization and chromosome separation during mouse oocyte maturation, fertilization, and early cleavage.Mol. Reprod. Dev. 2005; 71: 256-261Crossref PubMed Scopus (38) Google Scholar]. However, unlike mitosis, wherein the contractile ring encircles the cell equator, the polar body ring assembles as a discoid cortical washer. Here we show that in Caenorhabditis elegans, the meiotic contractile ring transforms during closure from a disc above the spindle to a cylinder around the spindle midzone. The meiotic midbody tube comprises stacked cytoskeletal rings. This topological transition suggests a novel mechanism for constriction of an initially discoid cytokinetic ring. Analysis of mouse PBE indicates that midbody tube formation is a conserved process. Depletion of the scaffold protein anillin (ANI-1) from C. elegans results in large and unstable polar bodies that often fuse with the oocyte. Anillin is dispensable for contractile ring assembly, initiation, and closure but is required for the meiotic contractile ring to transform from a disc into a tube. We propose that cytoskeletal bundling by anillin promotes formation of the midbody tube, which ensures the fidelity of PBE.