p90Rsk is required for G1 phase arrest in unfertilized starfish eggs

Abstract

DEVELOPMENT 1823 RESEARCH ARTICLE INTRODUCTIONThe female gamete of most animals arrests in the meiotic cell cycle while awaiting fertilization, and thus parthenogenesis is prevented. Depending on the organism, this arrest occurs at the beginning of meiosis I, metaphase of meiosis I, metaphase of meiosis II (meta-II) or the pronucleus stage after the completion of meiosis II (Sagata, 1996). How each of these different meiotic cell cycle arrests is executed and whether there is a common molecular principle are key issues in cell cycle arrest.The meta-II arrest that is observed in most of unfertilized vertebrate eggs has been most extensively studied. The activity that keeps eggs arrested in meta-II was first identified in the amphibian Rana pipiens and was called cytostatic factor (CSF) (Masui and Markert, 1971). Later studies established that the Mos-MAPK (mitogen-activated protein kinase) pathway is an essential core component of CSF in Xenopus and mouse eggs (Sagata et al., 1989;Haccard et al., 1993;Shibuya and Ruderman, 1993;Colledge et al., 1994;Hashimoto et al., 1994;Verlhac et al., 1996) (for reviews, see Sagata, 1996;Masui, 2000;Kishimoto, 2003;. The Mos-MAPK pathway maintains the activity of cyclin B-Cdc2 kinase at an elevated level (Yamamoto et al., 2005), and thereby arrests the cell cycle at meta-II in mature eggs of frog and mouse, resulting in the prevention of parthenogenetic activation.By contrast, unfertilized mature eggs of echinoderms, including starfish and sea urchin, are arrested at the pronucleus stage. Nonetheless, the same Mos-MAPK pathway causes the G1 phase arrest at the pronucleus stage in starfish Asterina pectinifera eggs (Tachibana et al., 1997;Tachibana et al., 2000) (see Kishimoto, 2004). Mature starfish eggs lacking in Mos or MAPK activity are activated parthenogenetically in the absence of fertilization. In unfertilized sea urchin eggs, MAPK is also responsible for the G1 arrest (Carroll et al., 2000), and it is plausible that a sea urchin homolog of Mos might be present and function upstream of MAPK.Considering the different arrest phases in frog and mouse versus starfish and sea urchin eggs, it is likely that a downstream effector of the Mos-MAPK pathway should determine the arrest phase. In Xenopus eggs, Rsk (p90 ribosomal S6 kinase) generates the CSF activity, immediately downstream of MAPK (Bhatt and Ferrell, Jr, 1999;Gross et al., 1999). Constitutively active forms of Rsk induce metaphase arrest independently of the activation of the Mos-MAPK pathway, while the metaphase arrest fails to occur after depletion of Rsk. In mouse eggs, however, Dumont et al. (Dumont et al., 2005) reported recently that Rsk is not involved in meta-II arrest, even though Rsk is activated during mouse meiotic cycles (Kalab et al., 1996). Mouse eggs from the triple Rsk knockout normally arrest at meta-II, and constitutively active mutant forms of Rsk do not restore meta-II arrest in mos-deficient oocytes. Thus, it is intriguing whether the G1 arrest in unfertilized starfish eggs requires Rsk activit...

Initiation of DNA replication after fertilization is regulated by p90Rsk at pre-RC/pre-IC transition in starfish eggs

“…In some organisms, including Drosophila and echinoderms (4-6), fertilization is not a prerequisite for the completion of meiosis, but required to trigger entry into the first S phase and the subsequent cleavage cycles. In starfish Asterina pectinifera (renamed to Patiria pectinifera in 2007 at the NCBI Taxonomy Browser), the Mos-MAPK (mitogen-activated protein kinase)-Rsk (p90 ribosomal S6 kinase, p90Rsk) pathway causes the G1-phase arrest at the pronucleus stage (6)(7)(8)(9)(10). Fertilization induces degradation of Mos to shutdown this pathway, leading to the first S phase with no requirement of new protein synthesis.…”

Erk2in Ovarian Development of Green Mud CrabScylla paramamosain

“…In starfish, which also spawn M I arrest oocytes, M I pause was maintained by ERK as well as low intracellular pH (*7.0) as recorded by Usui et al (2008). Moreover, the ERK transduction pathway was reported for involving in M I arrest (Usui et al, 2008), M I-M II transition (Tachibana et al, 2000), pronucleus stage arrest, and the eventual fate decision of starfish oocytes (Kishimoto, 2004;Sadler et al, 2004;Mori et al, 2006). Based on the information just outlined and on our experiments, we deduce that ERK in crab oocytes may participate in events before or around M I since the Sp-erk2 mRNA was strongly distributed in oocytes in relatively mature and mature ovarian tissues of GSI 7.9 and 10.43.…”

Phospho-Signaling at Oocyte Maturation and Fertilization: Set Up for Embryogenesis and Beyond Part I. Protein Kinases

“…Some S6Ks have been identified and characterized for example in progesterone-and insulin-treated Xenopus eggs termed S6K II (S6K II, p92) different from S6K I (Erikson et al 1987), differential role in Xenopus embryogenesis (S6K; p70) (Schwab et al 1999), in Rana oocytes (S6K; p83) (Byun et al 2002), in porcine oocytes (Sugiura et al 2002), and G1 phase after completion of meiosis II in starfish unfertilized eggs (Mori et al 2006) but not in mouse oocytes (Dumont et al 2005). S6K (p90 Rsk ) inhibits the degradation of cyclin B by anaphase-promoting complex/cyclosome (APC/C) and results the second meiotic metaphase arrest .…”