Inhibition of maturation and metabolism in rat oocytes by cyclic AMP

Magnusson, Claes; Hillensjø, Torbjörn

doi:10.1002/jez.1402010117

Cited by 131 publications

(43 citation statements)

References 16 publications

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“…A high level of cAMP, generated from a Gs-coupled oocyte receptor, is needed to maintain arrest in fully grown oocytes (Cho et al, 1974;Magnusson and Hillensjo, 1977;Bornslaeger et al, 1986;Mehlmann et al, 2002;Freudzon et al, 2005). This is enhanced by cGMP from the surrounding cumulus cells, which inhibits phosphodiesterase 3A (PDE3A) activity, preventing cAMP hydrolysis (Sela-Abramovich et al, 2008;Norris et al, 2009;Vaccari et al, 2009;Zhang et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes

et al. 2011

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FZR1, an activator of the anaphase-promoting complex/cyclosome (APC/C), is recognized for its roles in the mitotic cell cycle. To examine its meiotic function in females we generated an oocyte-specific knockout of the Fzr1 gene (Fzr1Δ/Δ). The total number of fully grown oocytes enclosed in cumulus complexes was 35-40% lower in oocytes from Fzr1Δ/Δ mice and there was a commensurate rise in denuded, meiotically advanced and/or fragmented oocytes. The ability of Fzr1Δ/Δ oocytes to remain prophase I/germinal vesicle (GV) arrested in vitro was also compromised, despite the addition of the phosphodiesterase milrinone. Meiotic competency of smaller diameter oocytes was also accelerated by Fzr1 loss. Cyclin B1 levels were elevated ~5-fold in Fzr1Δ/Δ oocytes, whereas securin and CDC25B, two other APC/CFZR1 substrates, were unchanged. Cyclin B1 overexpression can mimic the effects of Fzr1 loss on GV arrest and here we show that cyclin B1 knockdown in Fzr1Δ/Δ oocytes affects the timing of meiotic resumption. Therefore, the effects of Fzr1 loss are mediated, at least in part, by raised cyclin B1. Thus, APC/CFZR1 activity is required to repress cyclin B1 levels in oocytes during prophase I arrest in the ovary, thereby maintaining meiotic quiescence until hormonal cues trigger resumption.

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Section: Introductionmentioning

confidence: 99%

The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes

et al. 2011

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“…Maintenance of elevated cyclic adenosine monophosphate (cAMP) in oocytes is essential for sustaining meiotic arrest (2)(3)(4)(5)(6). After the LH surge, activation of an oocyte cAMP phosphodiesterase (PDE3A) reduces cAMP levels within the oocytes and activates the pathways culminating in GVB (7)(8)(9).…”

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confidence: 99%

Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes

Wigglesworth

Lee

O’Brien

et al. 2013

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

173

132

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Coordinated regulation of oocyte and ovarian follicular development is essential for fertility. In particular, the progression of meiosis, a germ cell-specific cell division that reduces the number of chromosomes from diploid to haploid, must be arrested until just before ovulation. Follicular somatic cells are well-known to impose this arrest, which is essential for oocyte-follicle developmental synchrony. Follicular somatic cells sustain meiotic arrest via the natriuretic peptide C/natriuretic peptide receptor 2 (NPPC/ NPR2) system, and possibly also via high levels of the purine hypoxanthine in the follicular fluid. Upon activation by the ligand NPPC, NPR2, the predominant guanylyl cyclase in follicular somatic cells, produces cyclic guanosine monophosphate (cGMP), which maintains meiotic arrest after transfer to the oocyte via gap junctions. Here we report that both the NPPC/NPR2 system and hypoxanthine require the activity of inosine monophosphate dehydrogenase (IMPDH), the rate-limiting enzyme required for the production of guanylyl metabolites and cGMP. Furthermore, oocyte-derived paracrine factors, particularly the growth differentiation factor 9-bone morphogenetic protein 15 heterodimer, promote expression of Impdh and Npr2 and elevate cGMP levels in cumulus cells. Thus, although the somatic compartment of ovarian follicles plays an essential role in the maintenance of oocyte meiotic arrest, as has been known for many years, this function of the somatic cells is surprisingly regulated by signals from the oocyte itself. F ertility in mammals depends on the coordinated development of ovarian follicles and the oocytes contained within them. The ovulation of oocytes by Graafian follicles must coincide with oocyte meiotic progression. Meiosis is a germ cell-specific cell division that reduces the number of chromosomes from diploid to haploid. In mammals, oocytes are arrested at the diplotene stage (diploid) of meiosis until the surge of luteinizing hormone (LH) from the pituitary gland initiates the ovulatory process. The LH surge initiates the resumption of meiosis and its progression to the metaphase of the second meiotic division, and these haploid oocytes (eggs) are ovulated into the oviduct to await fertilization. Ever since the classic experiments of Pincus and Enzmann (1) in the 1930s, it has been widely accepted that follicular somatic cells of Graafian follicles maintain the fully grown oocytes in meiotic arrest until the LH surge: Removing them from follicles for culture in a supportive medium before the surge results in an LH-independent resumption of meiosis. Thus, isolated oocytes resume meiosis simply because they have been separated from the inhibitory effect of follicular somatic cells. The mechanisms by which these cells maintain oocyte meiotic arrest have been the subject of numerous studies over the last 75 y.Oocytes arrested at the diplotene stage are referred to as germinal vesicle (GV)-stage oocytes, and the dissolution of the oocyte nuclear envelope, often referred to as germinal vesic...

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“…La maturation normale de l'ovocyte dépend de la transmission de signaux entre les cellules de la granulosa et l'ovocyte. Nous avons étudié l'effet d'une inhibition W7) n'a modifié qualitativement la Hillensjb, 1977;Dekel and Beers, 1978; amphibia: reviewed by Maller, 1983). This is based on the finding that cyclic AMP derivatives, such as dibutyryl cyclic AMP (dbcAMP), and activators of adenylate cyclase, like forskolin and cholera toxin, or inhibitors of phosphodiesterase, like 3-isobutyl-l-methylxanthine, inhibit germinal vesicle breakdown (GVBD).…”

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confidence: 99%