Sperm centriolar factors and genetic defects that can predict pregnancy

Abstract

The human sperm centrosome, comprising the two morphologically distinct centrioles and associated pericentriolar materials, plays a crucial role in fertilization and early embryonic development after fertilization. Once inside the oocyte, the sperm centrosome serves as a microtubule-organizing center, orchestrating mitotic spindle formation, chromosome segregation, and syngamy. Abnormalities of the sperm centrosome can lead to abnormal embryonic development and embryonic chromosomal instability, and are associated with pregnancy loss. Recent research has shed light on the molecular composition, regulation, and function of this vital organelle. Understanding the intricacies of the sperm centrosome is crucial for elucidating the mechanisms underlying successful fertilization and early embryonic development, as well as addressing infertility and developmental disorders associated with centrosomal defects. The human sperm centrosome, comprising the two morphologically distinct centrioles and associated pericentriolar materials, plays a crucial role in fertilization and early embryonic development after fertilization. Once inside the oocyte, the sperm centrosome serves as a microtubule-organizing center, orchestrating mitotic spindle formation, chromosome segregation, and syngamy. Abnormalities of the sperm centrosome can lead to abnormal embryonic development and embryonic chromosomal instability, and are associated with pregnancy loss. Recent research has shed light on the molecular composition, regulation, and function of this vital organelle. Understanding the intricacies of the sperm centrosome is crucial for elucidating the mechanisms underlying successful fertilization and early embryonic development, as well as addressing infertility and developmental disorders associated with centrosomal defects. In 1678, Leeuwenhoek described what he identified as “animalcules” in human semen, changing the prevailing belief that all animals originated exclusively from eggs (1Schierbeek A. The collected letters of Antoni van Leeuwenhoek; an appeal to the scientific world.Antonie Leeuwenhoek. 1953; 19: 181-188Crossref PubMed Scopus (4) Google Scholar). However, it took over a century for investigators including Bonnet, Spallanzani, and Reaumur to understand the role of the male gamete. This supposition paradoxically resulted in an overestimation of the male cell’s role and led to the belief that the human spermatozoon actually contained a little man identified as “homunculus” (2Hartsoeker N. Essai de dioptriques 1694.Google Scholar, 3Capanna E. Lazzaro Spallanzani: At the roots of modern biology.J Exp Zool. 1999; 285: 178-196Crossref PubMed Google Scholar), that once placed into a woman, would develop into a child (4Hill K.A. Hartsoeker's homonculus: a corrective note.J Hist Behav Sci. 1985; 21: 178-179Crossref PubMed Scopus (12) Google Scholar). This ideology of preformationism reflected the social credence of that time, focusing solely on attributing the entire role of procreation to men. This belief, however, was completely overturned after the early understanding of sexual reproduction and was later supported by the development of the in vitro fertilization (5Ferraretti A.P. Nygren K. Andersen A.N. de Mouzon J. Kupka M. Calhaz-Jorge C. et al.Trends over 15 years in ART in Europe: an analysis of 6 million cycles.Hum Reprod Open. 2017; 2017: hox012Crossref PubMed Google Scholar) procedure that paradoxically diminished the relevance of the spermatozoon, merely relegating it to a motile cell just capable of delivering the male genetic material to the site of fertilization. Semen analysis remains unchallenged as the primary assay used to evaluate the reproductive potential of male partners. This assay, which follows World Health Organization guidelines, focuses on sperm concentration and motility (6World Health OrganizationLaboratory manual for the examination and processing of human semen.6th ed. World Health Organization, Switzerland2021Google Scholar). Regarding sperm morphology, there have been relevant historical reappraisals, one of the most representative being the strict criteria introduced in 1986 (7Kruger T.F. Menkveld R. Stander F.S. Lombard C.J. Van der Merwe J.P. van Zyl J.A. et al.Sperm morphologic features as a prognostic factor in in vitro fertilization.Fertil Steril. 1986; 46: 1118-1123Abstract Full Text PDF PubMed Scopus (1081) Google Scholar). This was the first attempt to examine this gamete, considering not only the flagellum for its role in cell propulsion but also, most importantly, the shape and characteristics of the sperm head, such as the presence and characteristics of the acrosome, given its essential role in fertilization (6World Health OrganizationLaboratory manual for the examination and processing of human semen.6th ed. World Health Organization, Switzerland2021Google Scholar). A gradual revamping of the relevance of the male gamete in terms of the inheritance of genetic and epigenetic traits has been observed, mainly regarding the process of oocyte activation and the paternal contribution of a fundamental organelle responsible for proper chromosomal segregation within the resulting conceptus. The general components of mammalian spermatozoa are the head, midpiece, and flagellum, all of which are enveloped by the plasma membrane. Within the sperm head, the most recognizable organelle is the sperm nucleus, which contains the paternal genome that is highly compacted DNA wrapped around a protamine core, assuming a toroidal shape. Immediately anterior to the sperm nucleus is the acrosome, a membrane-bound vesicle derived from the Golgi apparatus. The acrosome stores proteolytic enzymes released during the acrosome reaction that occurs after capacitation. These acrosomal enzymes enable the male gamete to penetrate the cumulus cell matrix, and once broaching the glycoprotein zona pellucida, it fuses its equatorial segment with the oolemma microvilli (8Kaji K. Kudo A. The mechanism of sperm–oocyte fusion in mammals.Reproduction. 2004; 127: 423-429Crossref PubMed Scopus (72) Google Scholar). The proximal centriole is centrally located within the sperm midpiece and deeply inserted within the posterior portion of the nucleus. This organelle, composed of nine conjoined microtubule triplets, contributes to the proper development of the first mitotic spindle in humans and most other higher-order mammals. Posterior to the proximal centriole, the axoneme takes its origin from the distal centriole, serving as a template for the distal extension composed of nine jointed microtubule doublets surrounded by a central pair of microtubules. This highly conserved structure and associated components represent the nanomachine that drives sperm motility. The entire midpiece is encircled by aggregated sheets of mitochondria supported by dense outer fibers (9Pariz J.R. Rané C. Drevet J. Hallak J. Dysplasia of the fibrous sheath with axonemal and centriolar defects combined with lack of mitochondrial activity as associated factors of ICSI failure in primary ciliary dyskinesia syndrome.Int Braz J Urol. 2021; 47: 617-626Crossref PubMed Google Scholar). The acrosome is positioned over the anterior half of the sperm head as a cap-like secretory structure derived from the Golgi apparatus, enveloping a large proportion of the nuclear surface. The outer membrane of the acrosome fuses with the sperm plasma membrane, and subsequent vesiculation allows the release of proteolytic enzymes essential for the spermatozoon to traverse the cumulus oophorus. Once the spermatozoon reaches and penetrates the zona pellucida, it loses the outer acrosomal membrane, the segment for fusion with the oolemma R. A. spermatozoa fusion in the presence of Exp Zool. PubMed Scopus Google Scholar). 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