Atypical centrioles during sexual reproduction

Abstract

Centrioles are conserved, self-replicating, microtubule-based, 9-fold symmetric subcellular organelles that are essential for proper cell division and function. Most cells have two centrioles and maintaining this number of centrioles is important for animal development and physiology. However, how animals gain their first two centrioles during reproduction is only partially understood. It is well established that in most animals, the centrioles are contributed to the zygote by the sperm. However, in humans and many animals, the sperm centrioles are modified in their structure and protein composition, or they appear to be missing altogether. In these animals, the origin of the first centrioles is not clear. Here, we review various hypotheses on how centrioles are gained during reproduction and describe specialized functions of the zygotic centrioles. In particular, we discuss a new and atypical centriole found in sperm and zygote, called the proximal centriole-like structure (PCL). We also discuss another type of atypical centriole, the “zombie” centriole, which is degenerated but functional. Together, the presence of centrioles, PCL, and zombie centrioles suggests a universal mechanism of centriole inheritance among animals and new causes of infertility. Since the atypical centrioles of sperm and zygote share similar functions with typical centrioles in somatic cells, they can provide unmatched insight into centriole biology.

Dynamic changes in the transcriptome and methylome of Chlamydomonas reinhardtii throughout its life cycle

“…Early zygotes in C. reinhardtii also undergo dramatic changes in their cytoskeleton. Unlike the case in animals, where paternal but not maternal centrioles are contributed to zygotes (Avidor-Reiss et al, 2015), in C. reinhardtii, both parental basal bodies (structurally similar to centrioles) and flagella are retained initially in zygotes but eventually are disassembled and rebuilt during germination (Cavalier-Smith, 1976). Nonetheless, investigation of conserved zygotically up-regulated cytoskeletal proteins such as LF5 and SF-assemblin may shed light on more general mechanisms involved in controlling the dynamic behavior of flagella/cilia and basal bodies during cellular remodeling and life cycle transitions.…”

A comparative overview of the sperm centriolar complex in mammals and birds: Variations on a theme

“…When present, the PC in both vertebrate groups is short [0.3µm in the ostrich (Soley, 1993) and approximately 0.5µm in mammals as in somatic cells (Agircan et al, 2014)], lies partially within the implantation fossa at the base of the nucleus, and displays the characteristic pinwheel arrangement of microtubular triplets embedded in a ring of moderately electron-dense material (Avidor-Reiss et al, 2015;Sathananthan, 2012;Soley, 8 1993) (Fig. 2b).…”

“…For successful in vitro fertilisation (IVF) a thorough knowledge of sperm abnormalities was required and, based on patient studies, a number of obvious centriolar defects were identified that adversely affected fertility (Afzelius, 1996;Chemes, 2012;Chemes and Sedo, 2012;Moretti and Collodel, 2012;Zamboni, 1992). With the advent of intracytoplasmic sperm insemination (ICSI) it became clear that more subtle changes to the composition of the centrosome at a molecular level, not reflected as obvious structural anomalies, could adversely affect successful zygote formation 3 and subsequent embryogenesis (Avidor-Reiss et al, 2015;Chemes, 2012;Rawe, 2003, 2010;Sathananthan, 2012;Sathananthan et al, 1996).…”

“…Each centriole forms a hollow cylinder, the walls of which are composed of nine circularly arranged sets of triplet microtubules (Avidor-Reiss et al, 2 2015; Sathananthan, 2012;Sathananthan et al, 1996;Winey and O"Toole, 2014). In the centrosome a distinction can be made between the older (mother) centriole and the newly formed daughter centriole, although both organelles remain attached to each other (Bornens and Gönczy, 2014;Avidor-Reiss, 2015) Early ultrastructural studies on sperm from diverse species revealed the presence of a pair of centrioles located in the neck region of the cell. This observation initiated an intense and ongoing study on the structure and role of the centrosome during spermiogenesis and fertilization (Fawcett, 1971(Fawcett, , 1975.…”

“…The ultrastructural features of the centrosome have been documented in numerous publications. It consists essentially of a pair of centrioles aligned perpendicular to each other (forming a diplosome) and surrounded by an osmiophilic, fibro-granular matrix, the pericentriolar material (PCM) (Avidor-Reiss et al, 2015;Bornens and Gönczy, 2014;Chemes, 2012;Manandhar et al, 2005;Sathananthan, 2012;Sathananthan et al, 1996). Each centriole forms a hollow cylinder, the walls of which are composed of nine circularly arranged sets of triplet microtubules (Avidor-Reiss et al, 2 2015; Sathananthan, 2012;Sathananthan et al, 1996;Winey and O"Toole, 2014).…”