A membrane reticulum, the centriculum, affects centrosome size and function in Caenorhabditis elegans

Area of Science:

• Cell Biology
• Organelle Biology
• Developmental Biology

Background:

• Centrosomes, crucial for microtubule nucleation, consist of centrioles and pericentriolar material (PCM).
• While often considered membraneless, centrosomes in various cell types are associated with endoplasmic reticulum (ER)-derived membranes of unclear function.
• The structure and role of these associated membranes in early embryonic development remain largely unexplored.

Purpose of the Study:

• To investigate the structure and function of ER-derived membranes surrounding centrosomes in the early Caenorhabditis elegans (C. elegans) embryo.
• To determine the relationship between these membranes, centrosome components, and microtubule dynamics.
• To re-evaluate the membraneless nature of centrosomes in this model organism.

Main Methods:

• Volume electron microscopy (vEM) was employed to visualize the three-dimensional (3D) ultrastructure of centrosomes and associated membranes.
• Genetic manipulation was used to alter centriculum size and assess its impact on centrosome function.
• Microtubule dynamics and spindle morphology were analyzed in relation to centriculum characteristics.

Main Results:

• A 3D, ER-derived membrane reticulum, termed the centriculum, was identified surrounding C. elegans centrosomes.
• Centriculum formation depends on the presence of centrosomes and microtubules.
• Genetic expansion of the centriculum increased PCM, enhanced microtubule nucleation, and altered spindle width, indicating functional impact.

Conclusions:

• Centrosomes in the C. elegans early embryo are encased in a membrane meshwork (centriculum), challenging the membraneless organelle concept.
• The centriculum acts as a microtubule filter, regulating microtubule elongation.
• Centriculum-nuclear membrane fusion may contribute to nuclear envelope breakdown during mitosis.