C. elegans oocyte meiosis I involves a dynamic interplay of cellular structures, where researchers have uncovered the pivotal role of microtubules in regulating membrane ingression during polar body extrusion. This process is essential for maintaining genomic integrity during cell division, and the latest findings shed light on the delicate balance of forces required for successful polar body extrusion.
Professor Bruce Bowerman, along with Alyssa Quiogue, Dr. Eisuke Sumiyoshi, Adam Fries, and Dr. Chien-Hui Chuang from the Institute of Molecular Biology at the University of Oregon, have conducted a study demonstrating how microtubules interact with the actomyosin cortex to ensure proper cell division in C. elegans oocytes. Their research, published in the peer-reviewed journal PLOS Genetics, provides new insights into the mechanics of meiosis I.
During C. elegans oocyte meiosis I, a contractile ring formed by cortical actomyosin initiates membrane ingression, a critical step in polar body extrusion. Microtubules oppose this ingression, creating a balance that prevents excessive deformation of the oocyte membrane, which is crucial for proper chromosome segregation. Professor Bowerman explained, “Our findings show that microtubules may themselves provide a stiffness that counteracts the forces generated by cortical actomyosin, presumably with some cross-linking among themselves or with cortical actomyosin, ensuring that membrane ingression is regulated and does not compromise the integrity of the cell.”
The researchers employed advanced imaging techniques such as live cell imaging and spinning disk confocal microscopy, tagging proteins like CLS-2, KNL-1, and BUB-1 with fluorescent markers to track their distribution and interaction in real-time. This allowed them to observe how microtubule stability, influenced by treatments like nocodazole and taxol, affects membrane ingression. Professor Bowerman noted, “Our experiments with taxol and genetic backgrounds that elevate cortically associated microtubules showed that increased microtubule stability can suppress the membrane ingression defects seen in CLS-2 mutant oocytes,” indicating that promoting microtubule stability can correct ingression defects during meiosis.
Significant results from the study include observations that destabilizing or stabilizing microtubules with nocodazole or taxol respectively leads to altered membrane ingression. Specifically, destabilization results in excessive ingression, while stabilization reduces it. These findings underscore the importance of a well-regulated microtubule network in cell division.
The study also highlights that while actomyosin dynamics are critical, the underlying microtubules may provide the structural support necessary for balanced membrane ingression, although indirect signaling from microtubules to actomyosin has not been ruled out. This interaction between microtubules and actomyosin, whether direct or indirect, is essential for the proper functioning of the contractile ring that pinches off the polar body.
In conclusion, Professor Bowerman and the colleagues demonstrate the vital role of microtubules in opposing cortical actomyosin-driven membrane ingression during C. elegans meiosis I. This balance ensures that the oocyte cortex remains sufficiently stiff to allow proper cell division and polar body extrusion, a process crucial for genetic stability in developing embryos.
Journal Reference
Quiogue AR, Sumiyoshi E, Fries A, Chuang C-H, Bowerman B. Microtubules oppose cortical actomyosin-driven membrane ingression during C. elegans meiosis I polar body extrusion. PLoS Genet. 2023. DOI: https://doi.org/10.1371/journal.pgen.1010984