Structural Reorganization of the Sperm Flagellum Facilitates Fertilization by Inducing Motility Cessation

Alapfogalmak

The helical actin structure in the sperm midpiece undergoes a reorganization at the time of sperm-egg fusion, which triggers a decrease in midpiece diameter and motility arrest, both of which are required to complete the fusion process during fertilization.

Kivonat

The content investigates the structural and functional changes in the sperm flagellum after acrosome exocytosis (AE) and during the interaction with the eggs. The key findings are:

AE promotes a cessation of motility in a subset of sperm cells, which coincides with an increase in FM4-64 fluorescence in the midpiece.

AE is followed by a decrease in the midpiece diameter, which is observed using super-resolution microscopy, immunostaining, and scanning electron microscopy.

The contraction of the midpiece initiates preferentially at the proximal part of the flagellum, near the head-midpiece junction.

The midpiece contraction is driven by an increase in intracellular calcium ([Ca2+]i) that occurs concomitantly with a reorganization of the actin helicoidal cortex.

Live-cell imaging during in vitro fertilization showed that the midpiece contraction is required for motility cessation after sperm-egg fusion is initiated.

A decrease in [Ca2+]i in the midpiece following fusion precedes the midpiece contraction and motility arrest, which are necessary to complete the attachment and fusion between gametes.

Overall, the study provides the first evidence of the F-actin network's role in regulating sperm motility, adapting its function to meet the specific cellular requirements during fertilization.

Statisztikák

The midpiece diameter in acrosome-intact sperm was 0.731 ± 0.008 μm, while in acrosome-reacted sperm it was 0.694 ± 0.007 μm.

Idézetek

"The helical structure of polymerized actin undergoes a radical structural change at the time of sperm-egg fusion."
"A decrease in [Ca2+]i in the midpiece after fusion precedes midpiece contraction and the cessation of sperm motility that precedes sperm-egg fusion."

Főbb Kivonatok

Reorganization of the Flagellum Scaffolding Induces a Sperm Standstill During Fertilization

by Jablonski,M.... : www.biorxiv.org 06-22-2023

https://www.biorxiv.org/content/10.1101/2023.06.22.546073v4

Mélyebb kérdések

How do the structural changes in the sperm flagellum during fertilization impact the energetics and efficiency of the fusion process?

The structural changes in the sperm flagellum, particularly the contraction of the midpiece and the reorganization of the actin cytoskeleton, play a crucial role in the energetics and efficiency of the sperm-egg fusion process. As sperm approach the egg, they undergo acrosomal exocytosis (AE), which is accompanied by a significant increase in intracellular calcium levels. This calcium influx triggers a series of structural modifications in the flagellum, notably a decrease in the midpiece diameter and a reorganization of the helical actin network.
These changes are essential for motility cessation, which is a prerequisite for effective fusion with the egg. The contraction of the midpiece reduces the distance between the plasma membrane and the actin cytoskeleton, facilitating a more efficient interaction between the sperm and egg membranes. This close proximity is vital for the fusion process, as it allows for the necessary molecular interactions to occur without the interference of excessive motility.
Moreover, the energy dynamics are influenced by the transition from hyperactivated motility to a non-progressive state, which conserves energy and redirects it towards the fusion process. By halting motility, sperm can focus their energy on the biochemical events required for successful gamete fusion, thereby enhancing the overall efficiency of fertilization.

What are the potential implications of disrupting the actin cytoskeleton reorganization in the sperm midpiece for male infertility or assisted reproductive technologies?

Disruption of the actin cytoskeleton reorganization in the sperm midpiece could have significant implications for male infertility and assisted reproductive technologies (ART). The actin cytoskeleton is crucial for the structural integrity and functional dynamics of the sperm flagellum. If the reorganization of actin filaments is impaired, it may lead to inadequate midpiece contraction, resulting in persistent motility that prevents the sperm from effectively ceasing movement during the critical moments of fusion with the egg.
Such disruptions could manifest as reduced fertilization rates in natural conception scenarios, as sperm may fail to properly engage with the egg. In ART, where sperm selection and manipulation are critical, the inability to regulate motility through actin dynamics could hinder the success of procedures like in vitro fertilization (IVF). Sperm that cannot undergo the necessary structural changes may be less capable of penetrating the zona pellucida or completing the fusion process, leading to lower success rates in assisted reproductive techniques.
Furthermore, understanding the role of actin in sperm motility regulation could inform the development of targeted therapies or interventions aimed at enhancing sperm function in cases of male infertility. This knowledge could also lead to the design of novel sperm selection methods that prioritize motility characteristics linked to successful fertilization.

Could the insights gained from this study on sperm flagellum remodeling be extended to understand motility regulation in other cell types with specialized cytoskeletal structures?

Yes, the insights gained from this study on sperm flagellum remodeling can be extended to understand motility regulation in other cell types with specialized cytoskeletal structures. The fundamental principles of cytoskeletal dynamics, including the role of actin in motility regulation, are conserved across various cell types. For instance, similar mechanisms of actin reorganization and signaling pathways involving calcium ions are observed in other motile cells, such as immune cells (e.g., leukocytes) and certain types of epithelial cells.
In these cells, actin polymerization and depolymerization are critical for processes such as chemotaxis, where cells navigate towards chemical signals. The findings regarding the structural changes in the sperm flagellum during fertilization highlight the importance of precise cytoskeletal organization and its impact on motility. This knowledge can inform research into how other cell types regulate their movement in response to environmental cues or during developmental processes.
Moreover, the study of sperm motility can serve as a model for understanding the complexities of cytoskeletal interactions and their implications for cell behavior. By exploring the parallels between sperm and other motile cells, researchers can gain a deeper understanding of the molecular mechanisms that govern motility, potentially leading to advancements in regenerative medicine, cancer research, and tissue engineering, where cell movement plays a pivotal role.