A marked animal–vegetal polarity in the localization of Na⁺,K⁺‐ATPase activity and its down‐regulation following progesterone‐induced maturation

Abstract

The stage-VI Xenopus oocyte has a very distinct animal-vegetal polarity with structural and functional asymmetry. In this study, we show the expression and distribution pattern of Na(+),K(+) -ATPase in stage-VI oocytes, and its changes following progesterone-induced maturation. Using enzyme-specific electron microscopy phosphatase histochemistry, [(3) H]-ouabain autoradiography, and immunofluorescence cytochemistry at light microscopic level, we find that Na(+),K(+) -ATPase activity is mainly confined to the animal hemisphere. Electron microscopy histochemical results also suggest that polarized distribution of Na(+),K(+) -ATPase activity persists following progesterone-induced maturation, and it becomes gradually more polarized towards the animal pole. The time course following progesterone-induced maturation suggests that there is an initial up-regulation and then gradual down-regulation of Na(+),K(+) -ATPase activity leading to germinal vesicle breakdown (GVBD). By GVBD, the Na(+),K(+) -ATPase activity is completely down-regulated due to endocytotic removal of pump molecules from the plasma membrane into the sub-cortical region of the oocyte. This study provides the first direct evidence for a marked asymmetric localization of Na(+),K(+) -ATPase activity in any vertebrate oocyte. Here, we propose that such asymmetry in Na(+),K(+) -ATPase activity in stage-VI oocytes, and their down-regulation following progesterone-induced maturation, is likely to have a role in the active state of the germinal vesicle in stage-VI oocytes and chromosomal condensation after GVBD.

Oxidative Phosphorylation-linked Respiration in Individual Bovine Oocytes

“…This result correlates with microarray data in mouse oocytes showing that OXPHOS-involved transcripts were dramatically degraded in the transition from the GV to MII stage, suggesting a low rate of energy production in MII oocytes [22]. Indeed, it was observed in Xenopus oocytes that Na + /K + -ATPases are completely downregulated by germinal vesicle breakdown following progesterone-induce maturation [23]. Moreover, a constant high level of cyclic-adenosine monophosphate (cAMP) maintains meiotic arrest in fully grown oocytes, and this high level of cAMP is produced from ATP by an oocyte-specific G-protein coupled adenylyl cyclase [24,25].…”

The TMEM16A channel mediates the fast polyspermy block in Xenopus laevis

“…Although proteomics data reveal that X. laevis eggs express the xBEST2A channel, our data demonstrate that this channel does not contribute to the fast block. Based on its presence in the mature egg (Wühr et al, 2014) and its lack of contribution to the fast block, we speculate that xBEST2A is either desensitized or absent from the plasma membrane, as is the case for the plasma membrane Ca 2+ -ATPase (El-Jouni et al, 2005) and the Na + /K + ATPase (Mohanty and Gupta, 2012).…”

The Polarization of the G-Protein Activated Potassium Channel GIRK5 to the Vegetal Pole of Xenopus laevis Oocytes Is Driven by a Di-Leucine Motif

“…The endogenous nicotinic acetylcholine receptor channel predominates in the vegetal pole [30]; in contrast, calcium-dependent chloride channels [31] and exogenously expressed GABA receptors and sodium-voltage gated channels [32] are more abundant in the animal pole. With respect to the spatial distribution of ion transporters, the endogenous Na + /K + ATPase has been found in the animal pole [33].…”