A dynamic basal complex modulates mammalian sperm movement

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.

The human sperm basal body is a complex centrosome important for embryo preimplantation development

“…2A ). These data, in agreement with previous reports ( Fishman et al , 2018 ; Khanal et al , 2021 ), suggest that the human sperm basal body might be associated with centrosomal proteins. Altogether we conclude that the human sperm basal body includes two centrioles that show some basic features of conventional centrosomes, suggesting that it might not undergo a full process of centrosome reduction and establishing the foundation to perform a large scale approach to identify the human sperm PCM ( Manandhar et al , 2000 ; Manandhar and Schatten, 2000 ).…”

“…The localization of a subset of human sperm centrosomal proteins has been recently described using IF ( Fishman et al , 2018 ; Khanal et al , 2021 ) and our proteomic analysis further identified 7 out of 20 proteins that Fishman et al (2018) already described. Interestingly, we identified three centrosomal proteins that could not be detected by IF analysis (γ-tubulin chain 1, pericentrin and PCM 1), either because of technical limitations, such as accessibility in fixed samples, or their very low abundance, opening the possibility that many other centrosomal proteins may also be present in the basal body of the mature sperm.…”

“…Our study provides novel data that support an alternative mechanism. High-resolution microscopy has recently shown that the sperm distal centriole consists of an atypical, splayed microtubule structure that retains some centrosomal proteins ( Fishman et al , 2018 ; Khanal et al , 2021 ). Our super resolution analysis of centrin and acetylated tubulin localization in the human sperm basal body supports these findings.…”

“…The current model is that upon fertilization, the sperm atypical centrioles recruit PCM components stored in the oocyte cytoplasm to assemble a functional centrosome. A very limited number of studies have addressed this process in humans, except for a few reports showing that the human sperm shares many characteristics with those of other species ( Sathananthan et al , 1996 ; Simerly et al , 1999 ; Manandhar et al , 2000 ; Fishman et al , 2018 ; Khanal et al , 2021 ). Indeed, the human sperm distal centriole is also remodeled, although it retains a subset of centrosomal proteins, suggesting that sperm PCM reduction is not completed in humans ( Fishman et al , 2018 ; Khanal et al , 2021 ).…”

“…A very limited number of studies have addressed this process in humans, except for a few reports showing that the human sperm shares many characteristics with those of other species ( Sathananthan et al , 1996 ; Simerly et al , 1999 ; Manandhar et al , 2000 ; Fishman et al , 2018 ; Khanal et al , 2021 ). Indeed, the human sperm distal centriole is also remodeled, although it retains a subset of centrosomal proteins, suggesting that sperm PCM reduction is not completed in humans ( Fishman et al , 2018 ; Khanal et al , 2021 ). Nevertheless, the degree of conservation or loss of PCM components at the human sperm basal body, and the functional implications of these proteins for early embryonic development are still unresolved questions.…”