The effects of reduced oxygen tension on swine granulosa cell

Basini, Giuseppina; Bianco, Federico; Grasselli, Francesca; Tirelli, M.; Bussolati, Simona; Tamanini, Carlo

doi:10.1016/j.regpep.2004.02.013

Cited by 72 publications

(69 citation statements)

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“…Indeed, the partial pressure of oxygen is reported to decrease with increasing follicular size in women [6] and swine [7]. Furthermore, hCG regulates expression of hypoxiainducible factor (HIF)-1α in mammalian granulosa-lutein cellsand its responsive genes, which participate in different physiological processes in the ovary [8,9].…”

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confidence: 99%

Regulatory Effect of Hypoxia-Inducible Factor-1α on hCG-Stimulated Endothelin-2 Expression in Granulosa Cells from the PMSG-Treated Rat Ovary

Zhang

et al. 2012

Journal of Reproduction and Development

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Abstract. Endothelin (ET)-2 plays a crucial role in ovarian ovulation in mammals. The present study was designed to test the hypothesis that hypoxia-inducible factor (HIF)-1α-mediated transcriptional activation contributes to the increased expression of ET-2 gene in response to hCG in rat ovarian granulosa cells (GCs) during gonadotropin-induced superovulation. By realtime RT-PCR analysis, ET-2 mRNA expression was found to significantly increase in cultured ovarian GCs after treatment with hCG, or even N-carbobenzoxyl-L-leucinyl-L-leucinyl-L-norvalinal , while this increased ET-2 mRNA expression could also be blocked by ferrous ammonium sulfate (FAS) under human chorionic gonadotropin (hCG) treatment. Further analysis also found that these changes of ET-2 mRNA were consistent with HIF-1α expression or HIF-1 activity, and HIF-1α inhibitor echinomycin inhibited ovulation in rats. Taken together, these results indicate that ET-2 is transcriptionally activated by hCG through HIF-1α-mediated mechanism in GCs. This HIF-1α-induced transcriptional activation may be one of the important mechanisms mediating the increase of ET-2 expression in GCs during the gonadotropin-induced mammalian ovulatory process in vivo. Key words: Endothelin-2, Granulosa cells, Hypoxia-inducible factor-1α, Rat (J. Reprod. Dev. 58: [678][679][680][681][682][683][684] 2012) I n female rats, two pituitary gonadotropin hormones, FSH and LH, control reproductive cyclical events, including ovarian follicle maturation, rupture and release of fertilizable oocytes during a 4-day reproductive cycle in the initial stage of puberty. During each cycle, FSH stimulates a pool of preantral follicles to develop into mature follicles, while the ensuing surge of LH induces ovulation, through LH-activated downstream signaling pathways inthe preovulatory follicles and eventually triggers the release ofoocytes from these follicles [1,2]. At present, our understanding of the regulatory mechanisms controlling the growth and final differentiation of a mammalian follicle has advanced exponentially, but our understanding of even the most fundamental pathways is still not complete during these dynamic processes. Endothelin-2 (ET-2) was recently proposed as a granulosa cell-derived contractile signal that facilitates ovulation [3][4][5].Endothelin-2 (ET-2) is a small, 21 amino acid peptide that is produced by granulosa cells at the time of ovulation [3]. Expression of mRNA for ET-2, but not ET-1 or ET-3, is dramatically increased in the periovulatory follicle for only a very brief period of time (1-2 h) around ovulation, and blockade of endothelin receptor binding will delay/inhibit the process of follicular rupture [3]. This rather unique spatial-and temporal-specific pattern of mRNA expression suggests the involvement of direct signaling pathways to accurately coordinate controlled production of this peptide. Therefore, understanding of the regulatory mechanism controlling production of endothelin-2 (ET-2) becomes more and more important for further knowledge of the p...

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confidence: 99%

Regulatory Effect of Hypoxia-Inducible Factor-1α on hCG-Stimulated Endothelin-2 Expression in Granulosa Cells from the PMSG-Treated Rat Ovary

Zhang

et al. 2012

Journal of Reproduction and Development

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“…VEGF was found to have roles in the follicular development in 1992 by Ravindranath et al (Ravindranath et al 1992). HIF1 was recently found to have a role in the follicular development in pig (Basini et al 2004;Boonyaprakob et al 2005) and monkey . The lower pO2 in the FF in the large follicles than in the small follicles has been suggested to promote VEGF production via HIF1 in granulosa cells (Basini et al 2004).…”

Section: Roles Of Hypoxic Signaling In Follicular Development and Ovumentioning

confidence: 99%

“…The oxygen concentrations in the follicular fluid (FF) are lower in large follicles than in small follicles in cows (de Castro et al 2008), sows (Basini et al 2004) and women (Redding et al 2008). The oxygen concentration in the FF decreases with the oocyte maturation (Fischer et al 1992).…”

Section: Roles Of Hypoxic Signaling In Follicular Development and Ovumentioning

confidence: 99%

“…HIF1 was recently found to have a role in the follicular development in pig (Basini et al 2004;Boonyaprakob et al 2005) and monkey . The lower pO2 in the FF in the large follicles than in the small follicles has been suggested to promote VEGF production via HIF1 in granulosa cells (Basini et al 2004). On the other hand, in the primate ovary, nuclear immuno-staining of HIF1α is mostly absent in growing preantral and antral follicles, and is up-regulated in the granulosa cells at ovulation .…”

Section: Roles Of Hypoxic Signaling In Follicular Development and Ovumentioning

confidence: 99%

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Multiple roles of hypoxia in ovarian function: roles of hypoxia-inducible factor-related and -unrelated signals during the luteal phase

Nishimura

Okuda

2016

Reprod. Fertil. Dev.

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Promotion of Science (JSPS). 2 Abstract.There is increasing interest in the role of oxygen conditions in the microenvironment of organs, since the discovery of a hypoxia-specific transcription factor, hypoxia-inducible factor-1 (HIF1). Ovarian function has several phases that change day by day, including ovulation, follicular growth, corpus luteum formation and regression. These phases are regulated by many factors, such as pituitary hormones and local hormones including steroids, peptides and cytokines, as well as oxygen conditions. Hypoxia strongly induces angiogenesis because transcription of a potent angiogenic factor, vascular endothelial growth factor, is regulated by HIF1. Follicular development and luteal formation are accompanied by a drastic increase of angiogenesis assisted by the HIF1-VEGF signaling. Hypoxia is also one of the factors for inducing luteolysis by suppressing progesterone synthesis and by promoting apoptosis of luteal cells. This review focuses on recent studies for hypoxic conditions as well as HIF1-regulated genes and proteins in the regulation of ovarian function. Additional keywords Hypoxia, hypoxia-inducible factor IntroductionOvarian function has several phases that change day by day, including follicular growth, ovulation, luteal formation and regression. Follicles progress to ovulation through the proliferation of granulosa and theca cells. After ovulation, the corpus luteum (CL) develops accompanied by active angiogenesis, and when conception does not occur, regresses with the 3 decrease of progesterone (P4) synthesis and apoptosis of luteal cells. During the ovarian cycle, blood flow to the ovary changes, and affects the regulation of ovarian cycles Niswender et al. 1976;Ford and Chenault 1981;Wise et al. 1982;Magness et al. 1983;Acosta et al. 2002). Changes in ovarian blood flow result in the changes in the transport of nutrients, hormones and gases, including O2 to the ovary. In cows, ovarian blood flow has been reported to decrease during luteal regression, and to be kept at low levels during luteal formation after ovulation (Wise et al. 1982). Since a dominant follicle progress to ovulation during luteal regression (McCracken et al. 1999), follicular growth before ovulation occurs in parallel with the decrease of blood flow to the ovary. Furthermore, the oxygen content in ovarian venous blood begins to decrease at the late luteal stage (Wise et al. 1982). These findings indicate that the low oxygen condition (hypoxia) caused by the decreased blood supply is a characteristic part of the ovarian environment during follicular growth, ovulation and luteal formation. as VEGF (Forsythe et al. 1996; Kimura et al. 2001), endothelial nitric oxide synthase (eNOS) (Coulet et al. 2003), and heme oxygenase-1 (HOX-1) (Lee et al. 1997). VEGF stimulates angiogenesis and increases the permeability of blood vessels (Ferrara et al. 2003). eNOS and HOX-1 generate NO and carbon monoxide, which are potent vasodilatory substances that augment perfusion of the hypoxic tissue. At the cellular leve...

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“…Porcine granulosa cells represent a site of NO production (Grasselli et al 2002); the presence NO in physiology of the reproductive system of iNOS mRNA cannot be confirmed in granulosa cells from swine antral follicles (Grasselli et al 2001, Takesue et al 2001; eNOS mRNA expression in cultured porcine granulosa cells has been shown to depend upon FSH stimulation (Takesue et al 2001). Physiological hypoxia taking place during follicle growth could be an important factor inhibiting NO synthesis in swine granulosa cells (Basini et al 2004). In addition, it has been demonstrated that NO production by swine granulosa cells is modulated by physiological peptides (Basini et al 2011(Basini et al , 2014 as well as by endocrine disruptors (Santini et al 2009, Basini et al 2012.…”

Section: Regulation Of No Productionmentioning

confidence: 99%

Nitric oxide in follicle development and oocyte competence

Basini

Grasselli

2015

Reproduction

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Apart from its well-known role in regulating endothelial function, in mammals, nitric oxide (NO) is an important signaling molecule involved in many processes, regulating different biological functions. It has been demonstrated that NO plays a role in the physiology of the reproductive system, where it acts in controlling the activity of reproductive organs in both sexes. In the female of several animal species, experimental data suggest the presence of an intraovarian NO-generating system, which could be involved in the control of follicular development. The role of NO in regulating follicular atresia by apoptosis is still controversial, as a dual action depending mostly on its concentration has been documented. NO also displays positive effects on follicle development and selection related to angiogenic events and it could also play a modulatory role in steroidogenesis in ovarian cells. Both in monovulatory and poliovulatory species, the increase in PGE 2 production induced by NO via a stimulatory effect on COX-2 activity appears to be a common ovulatory mechanism. Considerable evidence also exists to support an involvement of the NO/NO synthase system in the control of meiotic maturation of cumulus-oocyte complexes.Reproduction (2015) 150 R1-R9

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The effects of reduced oxygen tension on swine granulosa cell

Cited by 72 publications

References 58 publications

Regulatory Effect of Hypoxia-Inducible Factor-1α on hCG-Stimulated Endothelin-2 Expression in Granulosa Cells from the PMSG-Treated Rat Ovary

Regulatory Effect of Hypoxia-Inducible Factor-1α on hCG-Stimulated Endothelin-2 Expression in Granulosa Cells from the PMSG-Treated Rat Ovary

Multiple roles of hypoxia in ovarian function: roles of hypoxia-inducible factor-related and -unrelated signals during the luteal phase

Nitric oxide in follicle development and oocyte competence

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