Toward the understanding of biology of oocyte life cycle in Xenopus Laevis: No oocytes left behind

Abstract

Background For the past more than 25 years, we have been focusing on the developmental and reproductive biology of the female gametes, oocytes, and eggs, of the African clawed frog Xenopus laevis. Methods The events associated with the life cycle of these cells can be classified into the four main categories: first, oogenesis and cell growth in the ovary during the first meiotic arrest; second, maturation and ovulation that occur simultaneously and result in the acquisition of fertilization competence and the second meiotic arrest; third, fertilization, that is sperm‐induced transition from egg to zygote; and fourth, egg death after spontaneous activation in the absence of fertilizing sperm. Main findings Our studies have demonstrated that signal transduction system involving tyrosine kinase Src and other oocyte/egg membrane‐associated molecules such as uroplakin III and some other cytoplasmic proteins such as mitogen‐activated protein kinase (MAPK) play important roles for successful ovulation, maturation, fertilization, and initiation of embryonic development. Conclusion We summarize recent advances in understanding cellular and molecular mechanisms underlying life cycle events of the oocytes and eggs. Our further intention is to discuss and predict potentially promising impact of the recent findings on the challenges facing reproductive biology and medicine, as well as societal contexts.

Bisphenol A Exposure Disrupts Organelle Distribution and Functions During Mouse Oocyte Maturation

“…During the development of oocytes, the excretion of the first polar body signals the completion of the first meiosis and indicates that the oocyte has reached the state of nuclear maturation ( Sen and Caiazza, 2013 ). Therefore, the excretion rate of the first polar body is a good indicator of the developmental ability of a mouse oocyte ( Sato and Tokmakov, 2020 ). First, we detected the effect of BPA treatment on the extrusion of the first polar body in a mouse oocyte.…”

“…Oocytes need adenosine triphosphate (ATP) to carry out meioses and other vital activities, and oocyte mitochondria are the major source of ATP during preimplantation embryonic development ( Babayev and Seli, 2015 ). During the first meiosis of the oocyte, the spindle that is formed by microtubules binds to homologous chromosomes and controls the synapsis and separation of homologous chromosomes until the first polar body is excreted ( Sato and Tokmakov, 2020 ). This process consumes a large amount of ATP, so the distribution of mitochondria is of great importance during the meiosis process.…”

Oocytes maintain ROS-free mitochondrial metabolism by suppressing complex I

“…a, A comparison between select reproductive traits of humans and Xenopus laevis, which live on average 76 years 59 and 15 years in captivity 60 , respectively. Xenopus oocytes have long been used in reproduction studies 61,62 , in part because they are more accessible and share many conserved features with human oocytes, such as (1) a long dormancy period: Xenopus oocytes arrest at late-stage I for several years. Moreover, a large population of early oocytes is maintained in adult female ovaries throughout most of its life-time, suggesting the presence of an oocyte reserve similar to humans [63][64][65] .…”

Dissection of the Ovulatory Process Using ex vivo Approaches

“…In frogs, no matured follicular oocytes can be observed in the ovary after ovulation, and all oocytes found in the genital tract during ovulation have completed GVBD, suggesting that GVBD and oocyte liberation from ovarian follicles are remarkably synchronized and coordinated in vivo . However, a great number of eggs dying by an apoptotic process are retained in the frog genital tract after ovulation ( Iguchi et al, 2013 ; Tokmakov et al, 2018 ; Sato and Tokmakov, 2020 ), indicating that oviposition rather than ovulation may be a bottleneck of the reproductive process in oviparous species.…”