Formation, architecture and polarity of female germline cyst in Xenopus

Abstract

Little is known about the formation of germline cyst and the differentiation of oocyte within the cyst in vertebrates. In the majority of invertebrates in the initial stages of gametogenesis, male and female germ cells develop in full synchrony as a syncytia of interconnected cells called germline cysts (clusters, nests). Using electron microscopy, immunostaining and three-dimensional reconstruction, we were able to elucidate the process of cyst formation in the developing ovary of the vertebrate Xenopus laevis. We found that the germline cyst in Xenopus contains 16 cells that are similar in general architecture and molecular composition to the cyst in Drosophila. Nest cells are connected by cytoplasmic bridges that contain ring canal-like structures. The nest cells contain a structure similar to the Drosophila fusome that that is probably involved in anchoring of the centrioles and organization of the primary mitochondrial cloud (PMC) around the centriole. We also find that in contrast to other organisms, in Xenopus, apoptosis is a rare event within the developing ovary. Our studies indicate that the processes responsible for the formation of female germline cysts and the establishment of germ cell polarity are highly conserved between invertebrates and vertebrates. The dissimilarities between Drosophila and Xenopus and the uniqueness of each system probably evolved through modifications of the same fundamental design of the germline cyst.

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…However, the observed pattern of microtubules does not permit full-length guidance, and oxygen gradients may play the major role in this context. For another example, a structure resembling the Drosophila fusome which is involved in anchoring centrioles and organizing the primary mitochondrial cloud around the centriole was found during female germline cyst development in Xenopus laevis (Kloc et al, 2004). Mitochondria also appear to be moved by microtubules during merozoite assembly in Plasmodium falciparum (Hopkins et al, 1999), and mitochondrial dysfunction results from abnormal microtubules in cytoplasmic male sterility of higher plants (Li et al, 2014, in conjunction with findings of Zhang et al, 2009).…”

Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown

“…Nobox deficiency in mice and perturbation of NOBOX homeodomain in women result in the premature ovarian failure (POF) syndrome characterized by postnatal oocyte loss and the replacement of follicles by fibrous tissue [1,2,6,8,10]. In mice, as in the majority of other animal species, mitotic divisions of primary oogonia, followed by incomplete cytokinesis, lead to the formation of germ cell cysts (nests, clusters) containing several oocytes connected by intercellular bridges [11][12][13]. Subsequently, the germ cell cysts break apart: somatic cells invade the cysts and separate and surround individual oocytes, resulting in the formation of individual ovarian follicles, which, in mammals, are called primordial follicles [11][12][13].…”

“…In mice, as in the majority of other animal species, mitotic divisions of primary oogonia, followed by incomplete cytokinesis, lead to the formation of germ cell cysts (nests, clusters) containing several oocytes connected by intercellular bridges [11][12][13]. Subsequently, the germ cell cysts break apart: somatic cells invade the cysts and separate and surround individual oocytes, resulting in the formation of individual ovarian follicles, which, in mammals, are called primordial follicles [11][12][13]. Histological studies of oocyte development in mice between the newborn stage and day 14 after birth showed that ovaries of Nobox +/− and Nobox −/− newborns have similar overall numbers of germ cell cysts and oocytes, indicating no overall germ cell loss [7].…”

Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body

“…In both Xenopus and Drosophila, the Balbiani body arises within interconnected germline cysts by the controlled assembly of organelles and germinal granule components at the time of follicle formation (26,36). Female mouse germ cells also generate cysts after reaching the genital ridge (37).…”