Abstract
Centrioles are subcellular organelles essential for normal cell function and development; they form the cell’s centrosome (a major cytoplasmic microtubule organization center) and cilium (a sensory and motile hair-like cellular extension). Centrioles with evolutionarily conserved characteristics are found in most animal cell types but are absent in egg cells and exhibit unexpectedly high structural, compositional, and functional diversity in sperm cells. As a result, the centriole’s precise role in fertility and early embryo development is unclear. The centrioles are found in the spermatozoan neck, a strategic location connecting two central functional units: the tail, which propels the sperm to the egg and the head, which holds the paternal genetic material. The spermatozoan neck is an ideal site for evolutionary innovation as it can control tail movement pre-fertilization and the male pronucleus’ behavior post-fertilization. We propose that human, bovine, and most other mammals–which exhibit ancestral centriole-dependent reproduction and two spermatozoan centrioles, where one canonical centriole is maintained, and one atypical centriole is formed–adapted extensive species-specific centriolar features. As a result, these centrioles have a high post-fertilization malfunction rate, resulting in aneuploidy, and miscarriages. In contrast, house mice evolved centriole-independent reproduction, losing the spermatozoan centrioles and overcoming a mechanism that causes miscarriages.
Highlights
IntroductionMiscarriage is a complex disease involving multiple factors in the sperm, egg, embryo, and uterus (Carbonnel et al, 2021; Klimczak et al, 2021; Thomas et al, 2021; Brandt et al, 2022; So et al, 2022)
We focus on the sperm centriole, a factor that has reemerged in the field of reproductive biology as a critical factor post-fertilization
This study demonstrates that the sperm tail and likely its centrioles contribute to embryo development
Summary
Miscarriage is a complex disease involving multiple factors in the sperm, egg, embryo, and uterus (Carbonnel et al, 2021; Klimczak et al, 2021; Thomas et al, 2021; Brandt et al, 2022; So et al, 2022). It was reported that horses, whose sperm have two centrioles, suffer from a high rate of aneuploidy in naturally occurring pregnancies (Shilton et al, 2020) Together, these recent studies point to a critical role of centrosome function in the embryo that is often jeopardized, resulting in a reduction in reproductive efficiency. Since the insect PC is atypical (proximal centriole-like (PCL) structure), one question that arises is whether it serves the same function as it does in mammals (Gottardo et al, 2015; Khire et al, 2016) This is not likely the case in Drosophila, as the DC connects directly to the tail axoneme and the head, while the PCL is found in the sperm neck cytoplasm to the side of the DC, and does not appear to be part of the same mechanical linkage. This may explain why donor sperm benefits older women in some cases (Bortoletto et al, 2021)
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