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

Abstract

The mechanism of conversion of the human sperm basal body to a centrosome after fertilization, and its role in supporting human early embryogenesis, has not been directly addressed so far. Using proteomics and immunofluorescence studies we show here that the human zygote inherits a basal body enriched with centrosomal proteins from the sperm, establishing the first functional centrosome of the new organism. Injection of human sperm tails containing the basal body into human oocytes followed by parthenogenetic activation, showed that the centrosome contributes to the robustness of the early cell divisions, increasing the probability of parthenotes reaching the compaction stage. In the absence of the sperm-derived centrosome, pericentriolar (PCM) components stored in the oocyte can form de novo structures after genome activation, suggesting a tight PCM expression control in zygotes. Our results reveal that the sperm basal body is a complex organelle which converts to a centrosome after fertilization, ensuring the early steps of embryogenesis and successful compaction. However, more experiments are needed to elucidate the exact molecular mechanisms of centrosome inheritance in humans.

The Centriole’s Role in Miscarriages

“…For a long time, it was thought that human sperm provided one functional centriole (the PC), one degraded or remnant centriole (the DC), and no pericentriolar material (PCM) to the egg ( Manandhar et al, 2005 ; Luo et al, 2013 ). However, recently it became evident that human, bovine, and probably most other mammalian sperm have two functional centrioles and PCM, though they may exhibit atypical designs ( Fishman et al, 2018 ; Amargant et al, 2021 ; Khanal et al, 2021 ; Leung et al, 2021 ). The PC displays slightly modified structure and composition, while the DC displays highly modified structure and composition.…”

“…Finally, in the absence of sperm centrioles, an activated egg can be stimulated to form a parthenote (an embryo developed from an unfertilized egg) ( Balakier and Casper, 1991 ). However, the mammalian parthenote does not reach live birth and usually dies by the blastocyst stage ( Wininger, 2004 ; Paffoni et al, 2007 ; Amargant et al, 2021 ). Parthenotes that undergo division eventually gain centrioles through the process of de novo centriole synthesis.…”

“…Amargant et al (2021) estimated that the human sperm carries 251 centrosomal proteins within its tail to the egg and found that one of these proteins (pericentrin) remains anchored to the sperm centrioles in the zygote ( Amargant et al, 2021 ). This study also showed that injection of human sperm tails into human oocytes followed by parthenogenetic activation results in more robust early cell divisions and improves the parthenote’s development.…”

“…Considering that the zygotic centrosome is a composite of sperm centrioles, male centrosomal proteins, and egg PCM proteins, the male and female contributions may compensate for each other’s deficiencies ( Schatten, 1994 ; Amargant et al, 2021 ). Therefore, having mildly abnormal sperm centrioles can also be exacerbated by weakened eggs, resulting in failed embryonic development.…”

Atypical Centriolar Composition Correlates with Internal Fertilization in Fish

“…The centriole near the nucleus is called the proximal centriole, while the more distant centriole, which also nucleates the flagellum, is called the distal centriole [ 31 ]. Both centrioles form a centrosome post-fertilization in the zygote [ 21 , 32 , 33 , 34 , 35 , 36 ].…”