The Maternal-Effect Gene cellular island Encodes Aurora B Kinase and Is Essential for Furrow Formation in the Early Zebrafish Embryo

Abstract

Females homozygous for a mutation in cellular island (cei) produce embryos with defects in cytokinesis during early development. Analysis of the cytoskeletal events associated with furrow formation reveal that these defects include a general delay in furrow initiation as well as a complete failure to form furrow-associated structures in distal regions of the blastodisc. A linkage mapping-based candidate gene approach, including transgenic rescue, shows that cei encodes the zebrafish Aurora B kinase homologue. Genetic complementation analysis between the cei mutation and aurB zygotic lethal mutations corroborate gene assignment and reveal a complex nature of the maternal-effect cei allele, which appears to preferentially affect a function important for cytokinesis in the early blastomeres. Surprisingly, in cei mutant embryos a short yet otherwise normal furrow forms in the center of the blastodisc. Furrow formation is absent throughout the width of the blastodisc in cei mutant embryos additionally mutant for futile cycle, which lack a spindle apparatus, showing that the residual furrow signal present in cei mutants is derived from the mitotic spindle. Our analysis suggests that partially redundant signals derived from the spindle and astral apparatus mediate furrow formation in medial and distal regions of the early embryonic blastomeres, respectively, possibly as a spatial specialization to achieve furrow formation in these large cells. In addition, our data also suggest a role for Cei/AurB function in the reorganization of the furrow-associated microtubules in both early cleavage- and somite-stage embryos. In accordance with the requirement for cei/aurB in furrow induction in the early cleavage embryo, germ plasm recruitment to the forming furrow is also affected in embryos lacking normal cei/aurB function.

aura/mid1ip1Lregulates the cytoskeleton at the zebrafish egg-to-embryo transition

“…1C), aura mutants are either fully syncytial or display pockets of cells aggregated atop a syncytial region (Fig. 1D, 256-cell and 1000-cell), resembling other cell division mutants (Pelegri et al, 1999;Dosch et al, 2004;Yabe et al, 2009). At a time coincident with the initiation of epiboly in Fig.…”

Kinesin-1 interacts with Bucky ball to form germ cells and is required to pattern the zebrafish body axis

“…During the first three cell cleavages, GP components accumulate at distal cleavage furrows and thereby become enriched in PGCs (Eno and Pelegri, 2013;Hashimoto et al, 2004;Knaut et al, 2000;Koprunner et al, 2001;Maegawa et al, 1999;Nair et al, 2013;Yabe et al, 2009;Yoon et al, 1997). The GP-RNAs nanos3 and vasa accumulated at the cleavage furrows of 4-cell-stage embryos ( Fig.…”

“…First, maternal-effect mutants that disrupt cytokinesis disrupt GP aggregation (Nair et al, 2013;Pelegri et al, 1999;Yabe et al, 2009). Second, during cytokinesis the cleavage furrow is flanked by MTs oriented perpendicular to the furrow, known as the furrow microtubule array (FMA), (Jesuthasan, 1998).…”

“…To date, zebrafish mutants disrupting GP assembly during early cleavages also perturb cleavages (Nair et al, 2013;Pelegri et al, 1999;Yabe et al, 2009). Both microtubule (MT) and F-actin networks are implicated in GP accumulation at cleavage furrows (Nair et al, 2013;Pelegri et al, 1999;Theusch et al, 2006;Yabe et al, 2009).…”

“…Both microtubule (MT) and F-actin networks are implicated in GP accumulation at cleavage furrows (Nair et al, 2013;Pelegri et al, 1999;Theusch et al, 2006;Yabe et al, 2009). MTs are enriched in distal cleavage furrows (Jesuthasan, 1998), and MT tips colocalize with GP-RNPs (Nair et al, 2013); however, it is unknown whether specific aggregation or stabilization factors exist and whether molecular motors are involved.…”