Electron tomography of mouse LINC complexes at meiotic telomere attachment sites with and without microtubules

Marie-Christin Spindler,Philip Kollmannsberger,Christian Stigloher,Frederik Helmprobst,Josef Redolfi,Ricardo Benavente

doi:10.1038/s42003-019-0621-1

Abstract

Telomere movements during meiotic prophase I facilitate synapsis and recombination of homologous chromosomes. Hereby, chromosome movements depend on the dynamic attachment of meiotic telomeres to the nuclear envelope and generation of forces that actively move the telomeres. In most eukaryotes, forces that move telomeres are generated in the cytoplasm by microtubule-associated motor proteins and transduced into the nucleus through the LINC complexes of the nuclear envelope. Meiotic LINC complexes, in mouse comprised of SUN1/2 and KASH5, selectively localize to the attachment sites of meiotic telomeres. For a better understanding of meiotic telomere dynamics, here we provide quantitative information of telomere attachment sites that we have generated with the aid of electron microscope tomography (EM tomography). Our data on the number, length, width, distribution and relation with microtubules of the reconstructed structures indicate that an average number of 76 LINC complexes would be required to move a telomere attachment site.

Highlights

Telomere movements during meiotic prophase I facilitate synapsis and recombination of homologous chromosomes
Tomography-based study of the telomere attachment sites as they are identified through the characteristic tight association of synaptonemal complexes with the nuclear envelope at this prophase stage
Meiotic chromosome movement throughout prophase I is essential for establishing genetic diversity in sexually reproducing

Summary

Introduction

Telomere movements during meiotic prophase I facilitate synapsis and recombination of homologous chromosomes. Chromosome movements depend on the dynamic attachment of meiotic telomeres to the nuclear envelope and generation of forces that actively move the telomeres. Forces that move telomeres are generated in the cytoplasm by microtubule-associated motor proteins and transduced into the nucleus through the LINC complexes of the nuclear envelope. LINC complexes are undoubtedly essential to meiotic telomere movement In somatic cells, they are distributed over the entire nuclear envelope. We were able to quantify the amount, length and width of meiotic LINC complexes This approach granted us to analyze the distribution of the filaments at attachment sites with and without microtubules, which resulted in a first estimation of the effective forces at telomere attachment sites

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