A dynamic basal complex modulates mammalian sperm movement

Sushil Khanal, Miguel Ricardo Leung, Abigail Royfman, Emily L. Fishman, Barbara Saltzman, Hermes Bloomfield-Gadêlha, Tzviya Zeev-Ben-Mordehai, Tomer Avidor-Reiss*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Reproductive success depends on efficient sperm movement driven by axonemal dynein-mediated microtubule sliding. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed. Centrioles are ancient organelles with a conserved architecture; their rigidity is thought to restrict microtubule sliding. Here, we show that, in mammalian sperm, the atypical distal centriole (DC) and its surrounding atypical pericentriolar matrix form a dynamic basal complex (DBC) that facilitates a cascade of internal sliding deformations, coupling tail beating with asymmetric head kinking. During asymmetric tail beating, the DC’s right side and its surroundings slide ~300 nm rostrally relative to the left side. The deformation throughout the DBC is transmitted to the head-tail junction; thus, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved as a dynamic linker coupling sperm head and tail into a single self-coordinated system.

Original languageEnglish
Article number3808
Pages (from-to)1-11
Number of pages11
JournalNature Communications
Volume12
Issue number1
DOIs
Publication statusPublished - 21 Jun 2021

Bibliographical note

Funding Information:
We would like to thank Kebron Assefa, Mohamed Baker Nawras, and Katriana Turner for their assistance throughout the study. We would like to thank The University of Toledo Instrumentation center for access to STORM microscopy. We thank the following people for providing sperm: Dr. Bo Harstine from Select Sires Inc. for donating the bovine sperm, Dr. Jie Xu lab at the University of Michigan for rabbit sperm, and Dr. Steve Pool at Fairfax Cryobank for human sperm, Dr. Heiko Henning at Utrecht University for providing bovine sperm for Cryo-ET. We thank Dr. Mihajlo Vanevic for cryo-EM computational support, Dr. Stuart Howes, Ingr Chris Schneijdenberg, and Johannes Meeldijk for management and maintenance of the Utrecht University EM Square facility. We thank the following people for editing and advising: Dr. Bo Harstine and Dr. Jadranka Loncarek. This work was supported by grant number R21 HD092700 from Eunice Kennedy Shriver National Institute of Child Health and Human Development and a grant from Select Sires Inc. This work was funded by NWO Start-Up Grant 740.018.007 to T.Z., and M.R.L. is supported by a Clarendon Fund-Nuffield Department of Medicine Prize Studentship.

Publisher Copyright:
© 2021, The Author(s).

Funding

We would like to thank Kebron Assefa, Mohamed Baker Nawras, and Katriana Turner for their assistance throughout the study. We would like to thank The University of Toledo Instrumentation center for access to STORM microscopy. We thank the following people for providing sperm: Dr. Bo Harstine from Select Sires Inc. for donating the bovine sperm, Dr. Jie Xu lab at the University of Michigan for rabbit sperm, and Dr. Steve Pool at Fairfax Cryobank for human sperm, Dr. Heiko Henning at Utrecht University for providing bovine sperm for Cryo-ET. We thank Dr. Mihajlo Vanevic for cryo-EM computational support, Dr. Stuart Howes, Ingr Chris Schneijdenberg, and Johannes Meeldijk for management and maintenance of the Utrecht University EM Square facility. We thank the following people for editing and advising: Dr. Bo Harstine and Dr. Jadranka Loncarek. This work was supported by grant number R21 HD092700 from Eunice Kennedy Shriver National Institute of Child Health and Human Development and a grant from Select Sires Inc. This work was funded by NWO Start-Up Grant 740.018.007 to T.Z., and M.R.L. is supported by a Clarendon Fund-Nuffield Department of Medicine Prize Studentship.

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