Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis

Abstract

Although centrosomes serve to organize microtubules in most cell types, oocyte spindles form and mediate meiotic chromosome segregation in their absence. Here, we use high-resolution imaging of both bipolar and experimentally-generated monopolar spindles in C. elegans to reveal a surprising organization of microtubules and chromosomes within acentrosomal structures. We find that homologous chromosome pairs (bivalents) are surrounded by microtubule bundles running along their sides, whereas microtubule density is extremely low at chromosome ends despite a concentration of kinetochore proteins on those regions. Further, we find that the chromokinesin KLP-19 is targeted to a ring around the center of each bivalent and provides a polar ejection force required for congression. Together, these observations create a new picture of chromosome/microtubule association in acentrosomal spindles and reveal a mechanism by which metaphase alignment can be achieved utilizing this organization. Specifically, we propose that: 1) Ensheathment by lateral microtubule bundles places spatial constraints on the chromosomes, thereby promoting biorientation, and 2) Localized motors mediate movement along these bundles, thereby promoting alignment.

The Chromosomal Passenger Complex Is Required for Meiotic Acentrosomal Spindle Assembly and Chromosome Biorientation

“…(E) A pathway for biorientation. (Rogers et al 2002;Wignall and Villeneuve 2009). The C. elegans CPC ring is a complex structure that, as in Drosophila, contains motor proteins (Klp-19) (Powers et al 2004) and is required for segregation of homologs at meiosis I (Wignall and Villeneuve 2009;Dumont et al 2010).…”

“…(Rogers et al 2002;Wignall and Villeneuve 2009). The C. elegans CPC ring is a complex structure that, as in Drosophila, contains motor proteins (Klp-19) (Powers et al 2004) and is required for segregation of homologs at meiosis I (Wignall and Villeneuve 2009;Dumont et al 2010). The importance of noncentromeric CPC in a variety of organisms suggests that the unique demands of acentrosomal meiosis have resulted in a meiosis-specific CPC/central spindle localization pattern with a conserved role in spindle assembly and chromosome segregation.…”

“…Some previous studies have suggested that chromosome alignment depends on lateral interactions during acentrosomal meiosis (Brunet et al 1999;Schuh and Ellenberg 2007;Wignall and Villeneuve 2009;Walczak et al 2010). However, an alternative model incorporates an important role for kinetochore microtubules (Dumont et al 2010).…”

Polar body emission

“…On the other hand, the holocentric C. elegans oocytes appear to employ lateral microtubules to align chromosomes in metaphase [Wignall and Villeneuve, 2009] and segregate chromosomes independently of kinetochores [Dumont et al, 2010].…”

Septin2 is modified by SUMOylation and required for chromosome congression in mouse oocytes

“…A recent study showed that congression on the acentrosomal spindle is driven primarily by movement of chromosomes along laterally associated microtubule bundles during meiosis, 37 suggesting that the mechanism of chromosome congression in meiosis is different from that in mitosis. Although septin2 has been shown to regulate chromosome congression 36 and cytokinesis, 33 its precise roles in meiosis are unknown.…”