RTN4-Mediated Endoplasmic Reticulum Remodeling Orchestrates Mitotic Organelle Inheritance and Spindle Dynamics

The endoplasmic reticulum (ER) is a pivotal orchestrator of cellular signaling and organelle positioning . Upon entering mitosis, it undergoes extensive morphological remodeling to ensure the faithful segregation of cellular components. Recent evidence highlights that RTN4 plays a non-decisive role in ER-mediated organelle positioning during interphase; however, RTN4-mediated ER reorganization is essential for the redistribution and inheritance of organelles during mitosis.

Experimental Quantification of Mitotic Partitioning

Knockout studies demonstrate that the loss of RTN4 leads to significant defects in the symmetric inheritance of both the ER and various organelles, as summarized in the table below:

Parameter Analyzed Conditions / Markers Analysis Type
ER Partitioning (Telophase) WT, RTN4 KO, RTN3 KO, REEP5 KO, DKO Fluorescence-intensity ratio
Organelle Distribution TOM20 (Mito), LAMP1 (Lyso), GM130 (Golgi), PEX14 (Perox) Fluorescence-intensity ratio
Spindle Positioning WT vs. RTN4 KO / RTN4B Mutants x-y plane deviation / z-axis angle (α)
Mitotic Progression Cell growth rate (CCK-8) / Time to anaphase Time-lapse imaging

Impact on Spindle Dynamics and Cell Proliferation

The disruption of RTN4-mediated ER reorganization significantly impairs mitotic spindle orientation. RTN4-knockout cells exhibit increased spindle orientation angles and astral microtubule defects, which resemble phenotypes often associated with spindle positioning abnormalities . These structural failures lead to a prolonged duration between nuclear envelope breakdown and anaphase onset. Furthermore, RTN4 deficiency results in elevated mitotic defects, including lagging chromosomes and chromosome bridges, which ultimately curtail cell proliferation rates.

Conclusion

In this study, we identify a fundamental mechanism of ER reorganization during early mitosis. The tubular ER-shaping protein RTN4 accumulates around centrosomes, driving the formation of a branched tubular ER network. This pericentrosomal remodeling is critical for establishing a symmetric ER distribution, which in turn facilitates the faithful inheritance of organelles and maintains the integrity of spindle dynamics. Our findings underscore that RTN4-mediated remodeling is not merely a morphological event but a functional requirement for accurate cell division and embryonic development.