Distinct roles for two C. elegans anillins in the gonad and early embryo.
Anillins are conserved proteins that are important for stabilizing and remodeling the actin cytoskeleton. Anillins have been implicated in cytokinesis in several systems and in cellularization of the syncytial Drosophila embryo. Here, we examine the functions of three C. elegans proteins with homology to anillin (ANI-1, ANI-2 and ANI-3). We show that ANI-1 and ANI-2 contribute to embryonic viability by performing distinct functions in the early embryo and gonad, respectively. By contrast, ANI-3 appears to be dispensable for embryonic development. ANI-1 is essential for cortical ruffling and pseudocleavage, contractile events that occur in embryos prior to mitosis. ANI-1 is also required for the highly asymmetric cytokinetic events that extrude the two polar bodies during oocyte meiosis, but is dispensable for cytokinesis following mitotic chromosome segregation. During both meiosis and mitosis, ANI-1 targets the septins, but not myosin II, to the contractile ring and does not require either for its own targeting. In contrast to ANI-1, ANI-2 functions during oogenesis to maintain the structure of the rachis, the central core of cytoplasm that connects the developing oocytes in the syncytial gonad. In ANI-2-depleted worms, oocytes disconnect prematurely from the defective rachis, generating embryos of varying sizes. Our results highlight specialization of divergent anillin family proteins in the C. elegans life cycle and reveal conserved roles for this protein family in organizing syncytial structures and cortical contractility.
Maddox
Amy Shaub
AS
Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, University of California-San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA. amaddox@ucsd.edu
Habermann
Bianca
B
Desai
Arshad
A
Oegema
Karen
K
D000818:Animals; D017173:Caenorhabditis elegans / Q000166:cytology / Q000196:embryology* / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D002454:Cell Differentiation; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism; D022081:Cell Surface Extensions; D003285:Contractile Proteins / Q000235:genetics / Q000378:metabolism*; D048749:Cytokinesis; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000196:embryology* / Q000378:metabolism*; D018507:Gene Expression Regulation, Developmental; D016678:Genome; D006066:Gonads / Q000166:cytology / Q000196:embryology* / Q000378:metabolism*; D008540:Meiosis; D008840:Microfilament Proteins / Q000235:genetics / Q000378:metabolism; D008938:Mitosis; D018995:Myosin Heavy Chains / Q000378:metabolism; D024462:Myosin Type II / Q000378:metabolism; D009865:Oocytes / Q000166:cytology / Q000378:metabolism; D034622:RNA Interference; D015996:Survival Rate; D013997:Time Factors
C502566:ANI-1 protein, C elegans; C502567:ANI-2 protein, C elegans; C502568:ANI-3 protein, C elegans; D029742:Caenorhabditis elegans Proteins; D003285:Contractile Proteins; D008840:Microfilament Proteins; C480837:NMY-2 protein, C elegans; C095886:anillin; D024462:Myosin Type II; D018995:Myosin Heavy Chains