MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans

• Published in: Developmental biology 2003-08, Vol.260 (1), p.245-259
• Main Authors: Yang, Hsin-ya, McNally, Karen, McNally, Francis J.
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Animals; Biological Transport, Active; Caenorhabditis elegans - genetics; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Calcium-Binding Proteins - deficiency; Cdc20 Proteins; Cell Cycle Proteins - metabolism; Cell Nucleus - metabolism; Chromosomes - metabolism; Cytoplasm - metabolism; Embryo, Nonmammalian; Female; Gene Expression Regulation, Developmental; Genes, Helminth; Helminth Proteins - genetics; Helminth Proteins - metabolism; Katanin; Meiosis - physiology; Microtubule-Associated Proteins - genetics; Microtubule-Associated Proteins - metabolism; Microtubules - metabolism; Mutation; Oocytes - cytology; Oocytes - physiology; RNA, Small Interfering - metabolism; Saccharomyces cerevisiae Proteins; Spindle Apparatus - physiology
• ISSN: 0012-1606; 1095-564X
• DOI: 10.1016/S0012-1606(03)00216-1

In most animals, successful segregation of female meiotic chromosomes involves sequential associations of the meiosis I and meiosis II spindles with the cell cortex so that extra chromosomes can be deposited in polar bodies. The resulting reduction in chromosome number is essential to prevent the generation of polyploid embryos after fertilization. Using time-lapse imaging of living Caenorhabditis elegans oocytes containing fluorescently labeled chromosomes or microtubules, we have characterized the movements of meiotic spindles relative to the cell cortex. Spindle assembly initiated several microns from the cortex. After formation of a bipolar structure, the meiosis I spindle translocated to the cortex. When microtubules were partially depleted, translocation of the bivalent chromosomes to the cortex was blocked without affecting cell cycle timing. In oocytes depleted of the microtubule-severing enzyme, MEI-1, spindles moved to the cortex, but association with the cortex was unstable. Unlike translocation of wild-type spindles, movement of MEI-1-depleted spindles was dependent on FZY-1/CDC20, a regulator of the metaphase/anaphase transition. We observed a microtubule and FZY-1/CDC20-dependent circular cytoplasmic streaming in wild-type and mei-1 mutant embryos during meiosis. We propose that, in mei-1 mutant oocytes, this cytoplasmic streaming is sufficient to drive the spindle into the cortex. Cytoplasmic streaming is not the normal spindle translocation mechanism because translocation occurred in the absence of cytoplasmic streaming in embryos depleted of either the orbit/CLASP homolog, CLS-2, or FZY-1. These results indicate a direct role of microtubule severing in translocation of the meiotic spindle to the cortex.