The Transformation of the Centrosome into the Basal Body: Similarities and Dissimilarities between Somatic and Male Germ Cells and Their Relevance for Male Fertility

Abstract

The sperm flagellum is essential for the transport of the genetic material toward the oocyte and thus the transmission of the genetic information to the next generation. During the haploid phase of spermatogenesis, i.e., spermiogenesis, a morphological and molecular restructuring of the male germ cell, the round spermatid, takes place that includes the silencing and compaction of the nucleus, the formation of the acrosomal vesicle from the Golgi apparatus, the formation of the sperm tail, and, finally, the shedding of excessive cytoplasm. Sperm tail formation starts in the round spermatid stage when the pair of centrioles moves toward the posterior pole of the nucleus. The sperm tail, eventually, becomes located opposed to the acrosomal vesicle, which develops at the anterior pole of the nucleus. The centriole pair tightly attaches to the nucleus, forming a nuclear membrane indentation. An articular structure is formed around the centriole pair known as the connecting piece, situated in the neck region and linking the sperm head to the tail, also named the head-to-tail coupling apparatus or, in short, HTCA. Finally, the sperm tail grows out from the distal centriole that is now transformed into the basal body of the flagellum. However, a centriole pair is found in nearly all cells of the body. In somatic cells, it accumulates a large mass of proteins, the pericentriolar material (PCM), that together constitute the centrosome, which is the main microtubule-organizing center of the cell, essential not only for the structuring of the cytoskeleton and the overall cellular organization but also for mitotic spindle formation and chromosome segregation. However, in post-mitotic (G1 or G0) cells, the centrosome is transformed into the basal body. In this case, one of the centrioles, which is always the oldest or mother centriole, grows the axoneme of a cilium. Most cells of the body carry a single cilium known as the primary cilium that serves as an antenna sensing the cell’s environment. Besides, specialized cells develop multiple motile cilia differing in substructure from the immotile primary cilia that are essential in moving fluids or cargos over the cellular surface. Impairment of cilia formation causes numerous severe syndromes that are collectively subsumed as ciliopathies. This comparative overview serves to illustrate the molecular mechanisms of basal body formation, their similarities, and dissimilarities, in somatic versus male germ cells, by discussing the involved proteins/genes and their expression, localization, and function. The review, thus, aimed to provide a deeper knowledge of the molecular players that is essential for the expansion of clinical diagnostics and treatment of male fertility disorders.

Development of the Connecting Piece in ODF1-Deficient Mouse Spermatids

“…A few other proteins were identified as essential components of the linkage complex that cause male infertility and sperm decapitation when missing [ 8 ]. Here, those proteins that are related to ODF1, either through similar subcellular distributions in the male germ cells or through interaction with ODF1, are of particular interest.…”

“…The formation of the connecting piece and the sperm flagellum is initiated in each case by one of the two paired centrioles. While the distal centriole, which is oriented perpendicular to the cell membrane, assembles the flagellum, the connecting piece is assembled by the proximal centriole [ 7 , 8 ]. The first sign of the development of the connecting piece is the accumulation of dense material on the wall of the proximal centriole, which is close to the nuclear membrane and perpendicular to the longitudinal axis of the sperm flagellum, and on the wall of the distal centriole.…”

Sun4 is a type II transmembrane protein of the spermatid inner nuclear membrane that forms heteromeric assemblies with Sun3 and interacts with Lamin B3

“…Even though sharing the typical molecular composition of a SUN domain protein, the actual localization of Sun4 and its de facto orientation within the NE were not entirely clear. Several previous studies have stated scenarios for Sun4 that are in apparent conflict with the classical topology of SUN domain proteins (Shao et al, 1999;Tapia Contreras and Hoyer-Fender, 2021;Yang et al, 2012;Yang et al, 2018). A couple of years ago, based on a Sun4 immunogold-labeling experiment, Shao et al (1999) showed that besides its nowadays accepted localization to the NE regions that are decorated by the manchette (Calvi et al, 2015;Gao et al, 2020;Pasch et al, 2015), Sun4 (= Spag4) appears to be also located within the axoneme.…”

The Male Mouse Meiotic Cilium Emanates from the Mother Centriole at Zygotene Prior to Centrosome Duplication

“…After meiosis, spermatids undergo dramatic morphological changes in order to transform into fully competent motile spermatozoa [34]. During this process, the sperm tail emerges from the mother centriole of the spermatid, which is thereby transformed into the basal body of the flagellum [35,36].…”