Functional anatomy of the mammalian sperm flagellum

Abstract

The eukaryotic flagellum is the organelle responsible for the propulsion of the male gamete in most animals. Without exception, sperm of all mammalian species use a flagellum for swimming. The mammalian sperm has a centrally located 9 1 2 arrangement of microtubule doublets and hundreds of accessory proteins that together constitute an axoneme. However, they also possess several characteristic peri-axonemal structures that make the mammalian sperm tail function differently. These modifications include nine outer dense fibers (ODFs) that are paired with the nine outer microtubule doublets of the axoneme, and are anchored in a structure called the connecting piece located at the base. The presence of the ODFs and connecting piece, and the absence of a basal body, dictate that physical forces generated by the dynein motors are transmitted to the base of the flagellum through the ODFs. Mammalian sperm flagella also possess a mitochondrial and a fibrous sheath that encircle most of the axoneme. These sheaths and the ODFs add mechanical rigidity to the flagellum creating the functional effect of increasing bend wavelength, which requires the entrainment of more dynein motors in the production of a single wave. The sheaths also act as a retinaculum and maintain the integrity of the central axoneme when large bending torques are generated by dynein. Large torque production is crucial to the process of hyperactivation and the unique motility transitions associated with effective fertilizing capacity. Consequently, these specialized anatomical features are essential for the effective interaction of sperm with the female reproductive tract and ovum. V C 2016 Wiley Periodicals, Inc.Key Words: axoneme; outer dense fibers; fibrous sheath; outer doublets; dynein; connecting piece; hyperactivation; sperm motility Introduction E ukaryotic cilia and flagella are highly conserved and ubiquitous organelles present in most animals, as well as many lower plants and eukaryotic protozoa. In the vertebrate lineage, the eukaryotic flagellum is universally employed to propel the male gamete. In the mammalian branch of the vertebrates, the sperm tail is always a modified flagellum with some characteristic accessory features that are added onto the basic 9 1 2 axoneme of microtubules found in most cilia and flagella. Figure 1 shows transmission electron micrographs (TEMs) of a mouse sperm flagellum in cross section at several positions along the length of the flagellum. The central axoneme is visible with its nine outer doublets surrounding a pair of single central microtubules (central pair or CP). Each of the outer microtubule doublets bears two rows of projections called the inner row and outer row of dynein arms. These arms are composed of the dynein motor proteins that power motility. The dynein arms are the source of the motive force that bends the flagellum. The dynein heavy chains (DHC) of the arms form bridges between the outer doublets and undergo a Mg-ATP driven power stroke that generates a sliding (or shearing) action between t...

TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa

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