A lumenal interrupted helix in human sperm tail microtubules

Davide Zabeo,Garry Morgan,Azusa Suzuki-Shinjo,Per O Widlund,Cindi L Schwartz,Johanna L Höög,John M Heumann

doi:10.1038/s41598-018-21165-8

Davide Zabeo, Garry Morgan + Show 5 more

Open Access

https://doi.org/10.1038/s41598-018-21165-8

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Abstract

Eukaryotic flagella are complex cellular extensions involved in many human diseases gathered under the term ciliopathies. Currently, detailed insights on flagellar structure come mostly from studies on protists. Here, cryo-electron tomography (cryo-ET) was performed on intact human spermatozoon tails and showed a variable number of microtubules in the singlet region (inside the end-piece). Inside the microtubule plus end, a novel left-handed interrupted helix which extends several micrometers was discovered. This structure was named Tail Axoneme Intra-Lumenal Spiral (TAILS) and binds directly to 11 protofilaments on the internal microtubule wall, in a coaxial fashion with the surrounding microtubule lattice. It leaves a gap over the microtubule seam, which was directly visualized in both singlet and doublet microtubules. We speculate that TAILS may stabilize microtubules, enable rapid swimming or play a role in controlling the swimming direction of spermatozoa.

Highlights

Cilia and flagella can be found on many animal, plant and protist cells
To study the structure of human flagella, we performed cryo-electron microscopy of the distal tip of human spermatozoa that were plunge-frozen in complete seminal fluid and we generated 55 cryo-electron tomograms on a total of 33 different intact human sperm tails (Table 1)
We have described a novel structure that we named Tail Axoneme Intra-Lumenal Spiral (TAILS), which is comprised of helical segments spaced every 8 nm

Summary

Introduction

Cilia and flagella can be found on many animal, plant and protist cells. It is an important cellular structure that can either act as an antenna[1], receiving signals from the environment, or provide cellular motility, such as in sperm tails. Woolley and Nickels (1985) observed that both the A-tubule and the B-tubule can transition into singlet microtubules at the flagellum tip, coining the term “duplex microtubules” for this singlet region arrangement[16] These duplex microtubules were later identified in human spermatozoa[3]. Electron microscopy and (cryo) electron tomography have shown that proteins localize to the inside of microtubules[33,34,35,36,37,38,39,40,41] These microtubule inner proteins (MIPs) are often found in dMTs and are all of unknown identity and function. Their specific localization and variable frequency suggest that they serve important regulatory functions for the microtubule cytoskeleton[5]

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