Abstract
Each human spermatozoon contains two remodeled centrioles that it contributes to the zygote. There, the centrioles reconstitute a centrosome that assembles the sperm aster and participate in pronuclei migration and cleavage. Thus, centriole abnormalities may be a cause of male factor infertility and failure to carry pregnancy to term. However, the precise mechanisms by which sperm centrioles contribute to embryonic development in humans are still unclear, making the search for a link between centriole abnormalities and impaired male fecundity particularly difficult. Most previous investigations into the role of mammalian centrioles during fertilization have been completed in murine models; however, because mouse sperm and zygotes appear to lack centrioles, these studies provide information that is limited in its applicability to humans. Here, we review studies that examine the role of the sperm centrioles in the early embryo, with particular emphasis on humans. Available literature includes case studies and case-control studies, with a few retrospective studies and no prospective studies reported. This literature has provided some insight into the morphological characteristics of sperm centrioles in the zygote and has allowed identification of some centriole abnormalities in rare cases. Many of these studies suggest centriole involvement in early embryogenesis based on phenotypes of the embryo with only indirect evidence for centriole abnormality. Overall, these studies suggest that centriole abnormalities are present in some cases of sperm with asthenoteratozoospermia and unexplained infertility. Yet, most previously published studies have been restricted by the laborious techniques (like electron microscopy) and the limited availability of centriolar markers, resulting in small-scale studies and the lack of solid causational evidence. With recent progress in sperm centriole biology, such as the identification of the unique composition of sperm centrioles and the discovery of the atypical centriole, it is now possible to begin to fill the gaps in sperm centriole epidemiology and to identify the etiology of sperm centriole dysfunction in humans.
Highlights
Centrioles are essential for animal development and physiology, as demonstrated by a variety of experiments that have tested the centriole’s role directly (Bettencourt-Dias et al, 2011)
While humans and many other mammals have centrioles in their spermatozoa and early embryos, mice, rats, and hamsters do not have recognizable centrioles in their spermatozoa and early embryos (Schatten et al, 1986; Sathananthan et al, 1996; Phillips et al, 2014). These major differences in centriole appearance raise the question: What exactly is the role of the centriole in human fertilization and early embryonic development?
This review focuses on the role of the mature sperm centrioles in the zygote, and it does not address the role of centrioles in germline development [reviewed in Riparbelli and Callaini (2011)]
Summary
Centrioles are essential for animal development and physiology, as demonstrated by a variety of experiments that have tested the centriole’s role directly (Bettencourt-Dias et al, 2011). While the timing for this is unknown in humans and non-murine animals, in mice, the first primary cilia have been observed in blastocysts with 64–100 cells, only after implantation on epiblast cells (Bangs et al, 2015) Based on these functions, sperm centrioles are widely expected to be essential in the embryo for development. Spermatozoa from humans and bovine, preloaded with functionblocking anti-proteasome antibody, resulted in disrupted sperm aster formation and pronuclear development/apposition of human oocytes, despite the lack of observable centriole structural deficits (Rawe et al, 2008) This suggests that spermatozoan proteasomes may play an important role in centriole contribution to zygote development. #1: 1–1.7 normal sperm + 7.9–16.8 acephalic sperm #2: 4.5 normal sperm); + 0.5 tail-less heads) + 4.5–34 isolated motile tails
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