Centriole behavior during meiosis in oocytes of the sea urchin Hemicentrotus pulcherrimus

Abstract

Ultrastructural changes in the maturing oocyte of the sea urchin Hemicentrotus pulcherrimus were observed, with special reference to the behavior of centrioles and chromosomes, using oocytes that had spontaneously started the maturation division process in vitro after dissection from ovaries. The proportion of oocytes entering the maturation process differed from batch to batch. In those eggs that accomplished the maturation division, it took ~4.5-5 h from the beginning of germinal vesicle breakdown to the formation of a second polar body. Serial sections revealed that a young oocyte before germinal vesicle breakdown had a pair of centrioles with procentrioles, located between the presumed animal pole and the germinal vesicle and accompanied by amorphous aggregates of moderately dense material and dense granules (granular aggregate). Just before germinal vesicle breakdown, a pair of fully grown centrioles located in the granular aggregate, which is present until this stage and then disappears, had already separated from another pair of centrioles. In meiosis I, each division pole had two centrioles, whereas in meiosis II each had only one. The two centrioles in the secondary oocyte separated into single units and formed the mitotic figure of meiosis II. The first polar body had two centrioles and the second had only one. The two centrioles in the first polar body did not form the mitotic figure nor did they separate at the time of meiosis II. These results indicate that, in sea urchins, duplication of the centrioles does not occur during the two successive meiotic divisions and the egg inherits only one centriole from the primary oocyte, confirming the results previously reported for starfish oocytes.

Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes

“…In contrast, in several other species, centrioles are eliminated during the actual meiotic divisions, and consequently meiotic spindles are astral. Although this was considered initially to be a specific feature of echinoderms (sea urchins, starfish, and sea cucumbers; Kato et al, 1990 ; Nakashima and Kato, 2001 ; Miyazaki et al, 2005 ), classic as well as recent evidence suggest that centrosomal meiotic spindles are widely spread across metazoan groups. In addition to echinoderms, meiotic spindles are astral in annelids, nemertea, and mollusks ( Longo and Anderson, 1969 ; Crowder et al, 2015 ), indicating that centriole elimination during the meiotic divisions is a widespread phenomenon.…”

Maintaining centrosomes and cilia

“…Finally, more recently, cilia were shown to produce extracellular vesicles (often referred to as exosomes) in an actin-dependent manner (Nager et al, 2017). These exosomes are biologically active and are required for hatching in Chlamydomonas (Wood et al, 2013) or are used in communication between individual C. elegans (Wang et al, 2014).…”

“…These exosomes are biologically active and are required for hatching in Chlamydomonas (Wood et al, 2013) or are used in communication between individual C. elegans (Wang et al, 2014). Exosomes can also return cilia to an inactive state after activation (Nager et al, 2017) and might be involved in maintaining other ciliary properties.…”

Atypical centrioles during sexual reproduction

“…During mammalian oogenesis, centrioles are present up to mid-Meiosis I (the pachytene stage), but are absent in the meiotic spindles of oocytes (Figure 5A ) (Szollosi et al, 1972 ; Sathananthan et al, 2006 ; Luksza et al, 2013 ). In contrast, in echinoderms (e.g., starfish and sea urchin), centrioles are present in female meiosis, and they are eliminated during polar body formation or lose their ability to duplicate (Sluder and Rieder, 1985a ; Sluder et al, 1989 ; Nakashima and Kato, 2001 ; Uetake et al, 2002 ; Shirato et al, 2006 ) (Figures 5B,C ). Altogether, regardless of whether maternal centrioles are present or absent during female meiosis, they neither function in zygote mitosis nor do they contribute to the embryo.…”