Second messenger signalling during hormone-induced<i>Xenopus</i>oocyte maturation

Cork, R. J.; Robinson, Kenneth R.

doi:10.1017/s0967199400002112

Cited by 11 publications

(9 citation statements)

References 94 publications

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“…Fully grown Xenopus oocytes can mature in response to insulin, as well as progesterone (18). The inability of growing oocytes to mature in response to insulin was reported to be due to multiple deficiencies CHAPTER 11/ MOLECULAR MECHANISMS OF O<XYTE MATURATION…”

Section: Oocyte Competencementioning

confidence: 99%

“…The most likely molecules involved in the signal transduction of Mlli are G-proteins and cAMP. A drop in intracellular cAMP levels and a subsequent decrease in A-kinase activity appear to be necessary for initiating oocyte maturation in a wide variety of species (18,133) as well as for a transition from mitosis to meiosis in fission yeast (168). In some species, however, an increase in cAMP is associated with the initial phase of oocyte maturation (W, 136,137), implicating binary functions of cAMP during oocyte maturation depending on the situations of oocytes.…”

Section: General and Species-specific Aspects Of 00cyfe Maturationmentioning

confidence: 99%

“…These results strongly suggest that a receptor for progesterone responsible for oocyte maturation exists on the oocyte plasma membrane, in striking contrast to the cytoplasmic or nuclear localisation of the wellcharacterised classical steroid receptors, including progesterone receptors involved in transcriptional regulation of the genes (13). The existence of a progesterone receptor on the oocyte surface was demonstrated by specific binding of a labelled ligand to membrane fractions obtained from fully grown frog oocytes (12,14,15), but the biochemical entity that represents the membrane-bound progesterone receptor is completely unknown, although a recent report suggests the presence on the oocyte plasma membrane of the same molecule as the cytoplasmic progesterone receptor (16).Cyclic AMP (cAMP) and ea 2 + have been best studied as molecules that mediate the MIH signal from the oocyte surface to cytoplasm (17,18). In this review, we only deal with the participation of cAMP in inducing oocyte maturation.…”

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confidence: 99%

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Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects

Yamashita

Mita

Yoshida

et al. 2000

Progress in Cell Cycle Research

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Stimulated by maturation-inducing hormone secreted from follicle cells surrounding the oocytes, fully-grown oocytes mature and become fertilisable. During maturation, immature oocytes resume meiosis arrested at the first prophase and proceed to the first or second metaphase at which they are naturally inseminated. Paying special attention to general and species-specific aspects, we summarise the mechanisms regulating the initial phase of oocyte maturation, from the reception of hormonal signals on the oocyte surface to activation of the maturationpromoting factor in the cytoplasm, in amphibians, fishes, mammals and marine invertebrates. INTRODUCfION TO OOCYTE MATURATIONThe life of multicellular organisms begins at fertilisation, the union of germ cells (the egg and the spermatozoon). The production and maturation of germ cells and their fusion are indispensable for the maintenance of a species beyond the limited longevity of individuals. Oocytes are produced in ovaries by the entry of mitotically proliferating oogonia into meiosis. Oocytes stop their meiotic cell cycle at the first prophase, during which they grow by the accumulation of substances necessary for early embryonic development (vitellogenesis). In many species, fullygrown postvitellogenic oocytes arrested at the first meiotic prophase are immature, and they are unable to be fertilised until they mature. The oocytes that have been induced to mature resume meiosis from the first prophase and proceed to the first or second metaphase, at which time, in many invertebrates and vertebrates, they are inseminated (1). During the course of maturation, oocytes undergo drastic morphological changes associated with progression of the meiotic cell cycle, among which breakdown of the oocyte nuclear envelope (germinal vesicle breakdown, GVBD) occurring at the prophase/metaphase transition is frequently regarded as a hallmark of the progress of maturation, although it does not necessarily mean the completion of maturation (Figure 1).Oocyte maturation is induced by sequential actions of three substances (2): gonadotropic hormone (GTH; or gonad-stimulating substance in starfish, GSS), maturation-inducing hormone (MIH; or maturationinducing substance, MIS) and maturation-promoting factor (MPF) (Figure 2). Two species of GTH, a luteinizing hormone (LH) and a follicle-stimulating hormone (FSH), are secreted from the pituitary gland in vertebrates. Both LH and FSH consist of two glycoproteinous subunits, a and ~ subunits; the former is also a component of the thyroid-stimulating hormone (ISH) and the latter characterises each hormone. FSH is responsible for oocyte growth, and LH triggers oocyte maturation by stimulating follicle cells surrounding the 115 oocytes to produce MIH. MIH in vertebrates is a steroid derivative and interacts with a membrane-bound receptor on the oocyte surface, and subsequent signal transduction from the surface to the cytoplasm is probably intermediated by GfP-binding proteins (Gproteins). The MIH signal finally results in the formation and activa...

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Section: Oocyte Competencementioning

confidence: 99%

Section: General and Species-specific Aspects Of 00cyfe Maturationmentioning

confidence: 99%

mentioning

confidence: 99%

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Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects

Yamashita

Mita

Yoshida

et al. 2000

Progress in Cell Cycle Research

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“…The steroid hormone progesterone is the mitogen that breaks this arrest, initiating resumption of the meiotic cell cycles and conversion of the immature oocyte into the mature, fertilizable egg (Masui, 1967; Schuetz, 1967). It has been known for more than 20 years that progesterone acts at or near the surface and activates the oocyte through a pathway that does not depend on transcription (reviewed by Smith, 1989; Cork and Robinson, 1994). Instead, progesterone initiates a poorly understood signaling pathway that leads to the translational recruitment of several stored mRNAs.…”

Section: Introductionmentioning

confidence: 99%

The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway

1998

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Quiescent Xenopus oocytes are activated by progesterone, which binds to an unidentified surface-associated receptor. Progesterone activates a poorly understood signaling pathway that results in the translational activation of mRNA encoding Mos, a MAP kinase kinase kinase necessary for the activation of MAP kinase and MPF, the resumption of meiosis, and maturation of the oocyte into the sperm-responsive egg. We have designed a screen to identify early signaling proteins based on the premise that some of these proteins would be phosphorylated or otherwise modified within minutes of progesterone addition. This screen has revealed Eg2, a Ser/Thr kinase. We find that Eg2 is phosphorylated soon after progesterone stimulation and provide evidence that it functions in the signaling pathway. Overexpression of Eg2 via mRNA microinjection shortens the time between progesterone stimulation and the appearance of new Mos protein, accelerates activation of MAP kinase and advances entry into the meiotic cell cycle. Finally, overexpression of Eg2 dramatically reduces the concentration of progesterone needed to trigger oocyte activation. These results argue that the kinase Eg2 is a component of the progesterone-activated signaling pathway that releases frog oocytes from cell cycle arrest.

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“…F ull-grown frog oocytes arrest at the G 2 ͞M border of meiosis I until exposed to progesterone, their physiological mitogen (reviewed in refs. [1][2][3][4]. Progesterone induces oocyte maturation, initiating oocyte activation, resumption of the meiotic cell cycles, and development into the mature, fertilizable egg.…”

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confidence: 99%

Identification of XPR-1, a progesterone receptor required for Xenopus oocyte activation

Tian

Kim

Heilig

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

159

114

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Quiescent full-grown Xenopus oocytes remain arrested at the G2͞M border of meiosis I until exposed to progesterone, their natural mitogen. Progesterone triggers rapid, nontranscriptional responses that lead to the translational activation of stored mRNAs, resumption of the meiotic cell cycles, and maturation of the oocyte into a fertilizable egg. It has long been presumed that progesterone activates the oocyte through a novel nontranscriptional signaling receptor. Here, we provide evidence that a conventional transcriptional progesterone receptor cloned from Xenopus oocytes, XPR-1, is required for oocyte activation. Overexpression of XPR-1 through mRNA injection increases sensitivity to progesterone and accelerates progesterone-activated cell cycle reentry. Injection of XPR-1 antisense oligonucleotides blocks the ability of oocytes to respond to progesterone; these oocytes are rescued by subsequent injection of XPR-1 or the human progesterone receptor PR-B. Antisense-treated oocytes can be activated in response to inhibition of protein kinase A, one of the earliest known changes occurring downstream of progesterone stimulation. These results argue that the conventional progesterone receptor also functions as the signaling receptor that is responsible for the rapid nontranscriptional activation of frog oocytes.

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Second messenger signalling during hormone-inducedXenopusoocyte maturation

Cited by 11 publications

References 94 publications

Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects

Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects

The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway

Identification of XPR-1, a progesterone receptor required for Xenopus oocyte activation

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