Evidence that the preovulatory rise in intrafollicular progesterone may not be required for ovulation in cattle

Li, Qinglei; Jimenez-Krassel, Fermin; Bettegowda, Anilkumar; Ireland, James J.; Smith, George W.

doi:10.1677/joe-06-0020

Cited by 24 publications

(10 citation statements)

References 46 publications

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“…In this system, LH increased PTGS2 and PLAU mRNA levels above those of time-matched controls at 6 to 12 h after challenge, which is consistent with the time course of human chorionic gonadotropin (hCG)/gonadotropin-releasing hormone (GnRH)-inducible increases in PTGS2 and PLAU mRNA abundance in cattle in vivo [38][39][40][41], although this is slightly earlier than in granulosa cells collected from preovulatory follicles and challenged with LH in vitro [42]. One caveat to the use of this culture system is that basal PTGS2 mRNA levels declined during the test period, which likely FIG.…”

Section: Discussionsupporting

confidence: 79%

Role of Angiotensin II in the Periovulatory Epidermal Growth Factor-Like Cascade in Bovine Granulosa Cells In Vitro1

Portela¹,

Zamberlam²,

Gonçalves³

et al. 2011

Biology of Reproduction

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Angiotensin II (AGT-2) induces follicular prostaglandin release in a number of species and ovulation in rabbits. Conversely, AGT-2 antagonists block ovulation in cattle. To determine the mechanism of action of AGT-2, we used a bovine granulosa cell model in which luteinizing hormone (LH) increased the expression of genes essential for ovulation in a time- and dose-dependent manner. The addition of AGT-2 to LH-stimulated cells significantly increased abundance of prostaglandin-endoperoxide synthase 2 (PTGS2) mRNA and protein, whereas AGT-2 alone had no effect. Upstream of PTGS2, AGT-2 increased abundance of mRNA encoding the epidermal growth factor-like ligands amphiregulin (AREG) and epiregulin (EREG) at 6 h posttreatment and abundance of a disintegrin and metalloprotease 17 (ADAM17), a sheddase, within 3 h of treatment. Inhibiting sheddase activity abolished the stimulatory effect of AGT-2 on AREG, EREG, and PTGS2 mRNA. The addition of selective AGT-2 antagonists to cells stimulated with LH plus AGT-2 demonstrated that AGT-2 did not act through the type 1 receptor and did not increase mitogen-activated protein kinase 3/1 phosphorylation. Combined with previous data from studies in vitro, we conclude that AGT-2 is an essential cofactor for LH in the early increase of ADAM expression/activity that induces the cascade of events leading to ovulation.

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Section: Discussionsupporting

confidence: 79%

Role of Angiotensin II in the Periovulatory Epidermal Growth Factor-Like Cascade in Bovine Granulosa Cells In Vitro1

Portela¹,

Zamberlam²,

Gonçalves³

et al. 2011

Biology of Reproduction

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“…Biological actions of JY-1 on bovine granulosa cells do not mimic the reported effects of the well known oocyte-specific growth factors GDF9 and BMP15 on bovine granulosa cell function (34,35). In vivo, the preovulatory gonadotropin (luteinizing hormone) surge results in decreased estradiol and increased progesterone levels in the follicular fluid of bovine preovulatory follicles (36), and preovulatory granulosa cells exit from the cell cycle and are transformed into nondividing terminally differentiated luteal cells capable of producing high levels of progesterone (37,38). In our culture studies, the increase in progesterone was accompanied by a suppression of the FSH-stimulated increase in granulosa cell numbers and estradiol production, mimicking the in vivo preovulatory follicular environment.…”

Section: Discussionmentioning

confidence: 95%

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

Bettegowda

Yao

Sen

et al. 2007

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

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Oocyte-specific gene products play a key role in regulation of fertility in mammals. Here, we describe the discovery, molecular characterization, and function of JY-1, a bovine oocyte-expressed gene shown to regulate both function of ovarian granulosa cells and early embryogenesis in cattle and characteristics of JY-1 loci in other species. The JY-1 gene encodes for a secreted protein with multiple mRNA transcripts containing an identical ORF but differing lengths of 3 UTR. JY-1 mRNA and protein are oocyte-specific and detectable throughout folliculogenesis. Recombinant JY-1 protein regulates function of follicle-stimulating hormone-treated ovarian granulosa cells, resulting in enhanced progesterone synthesis accompanied by reduced cell numbers and estradiol production. JY-1 mRNA of maternal origin is also present in early bovine embryos, temporally regulated during the window from meiotic maturation through embryonic genome activation, and is required for blastocyst development. The JY-1 gene has three exons and is located on bovine chromosome 29. JY-1-like sequences are present on syntenic chromosomes of other vertebrate species, but lack exons 1 and 2, including the protein-coding region, suggestive of species specificity in evolution and function of this oocyte-specific gene.T he oocyte is a key regulator of multiple aspects of female fertility, including ovarian follicular development and early embryogenesis (1). The advent of oocyte genomics and EST sequencing projects have led to a dramatic increase in our understanding about the identities and functions of oocytespecific genes in female reproduction (2, 3). However, inherent species-specific differences exist in the ovulation quota, follicular waves, duration of the ovarian cycle, and number of embryonic cell cycles required for embryonic genome activation (4) between the traditional animal model (polyovulatory mouse) versus monoovulatory species such as cattle and primates, including humans. Numerous examples suggest that oocytespecific genes identified in the mouse may not have identical functions in other species. For instance, Belclare and Cambridge ewes with naturally occurring heterozygous mutations in the GDF9 gene have an increased ovulation rate and litter size (5), but mice heterozygous for the GDF9 gene disruption exhibit no obvious phenotype (6). Similarly, Inverdale and Hanna strains of sheep with homozygous mutations in BMP15 are infertile (7, 8), whereas homozygous BMP15 mutant mice are subfertile with defects in ovulation and fertilization (9). Thus, comparative genomics approaches coupled to functional studies in nontraditional model systems are needed to address dissimilarities in transcriptome composition between model organisms and provide information on existence of genes or gene families that may play important regulatory roles in fertility in nonmurine models, including the human. With this goal in mind, we previously constructed a bovine oocyte cDNA library and sequenced a number of ESTs (2). A highly abundant transcript (designat...

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“…However, to our knowledge BZR expression in the bovine ovary has not been reported. It will be interesting to determine whether the increase in DBI makes a functional contribution to the increase in progesterone production accompanying the luteinization processes in bovine preovulatory follicles (Li et al 2007).…”

Section: Discussionmentioning

confidence: 99%

Gene expression profiling of bovine preovulatory follicles: gonadotropin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process

Jimenez-Krassel

Ireland

et al. 2009

Reproduction

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The molecular mechanisms of ovulation and luteinization have not been well established, partially due to lack of a comprehensive understanding of functionally significant genes up-regulated in response to an ovulatory stimulus and the signaling pathways involved. In the present study, transcripts increased in bovine preovulatory follicles following a GnRH-induced LH surge were identified using microarray technology. Increased expression of 368 and 878 genes was detected at 12 (368 genes) and 20 h (878 genes) following GnRH injection. The temporal, cell specific and prostanoid-dependent regulation of selected genes (ADAM10, DBI, CD36, MTSS1, TFG, and RABGAP1) identified from microarray studies and related genes (ADAM17 and AREG) of potential significance were also investigated. Expression of mRNA for DBI and CD36 was simultaneously up-regulated in theca and granulosa cells (GC) following the LH surge, whereas temporal regulation of ADAM10, MTSS1, TFG, and RABGAP1 was distinct in the two cell compartments and increased granulosa TFG and RABGAP1 mRNA were prostanoid dependent. AREG mRNA was increased in theca and GCs at 12 and 24 h following GnRH injection. ADAM17 mRNA was increased in theca, but reduced in GCs 24 h following GnRH injection. The increased ADAM17 and AREG mRNA were prostanoid dependent. ADAM10 and ADAM17 protein were increased specifically in the apex but not the base of preovulatory follicles and the increase in ADAM17 was prostanoid dependent. Results reveal novel information on the regulation of preovulatory gene expression and suggest a potential functional role for ADAM10 and ADAM17 proteins in the region of follicle rupture.

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Evidence that the preovulatory rise in intrafollicular progesterone may not be required for ovulation in cattle

Cited by 24 publications

References 46 publications

Role of Angiotensin II in the Periovulatory Epidermal Growth Factor-Like Cascade in Bovine Granulosa Cells In Vitro1

Role of Angiotensin II in the Periovulatory Epidermal Growth Factor-Like Cascade in Bovine Granulosa Cells In Vitro1

JY-1 , an oocyte-specific gene, regulates granulosa cell function and early embryonic development in cattle

Gene expression profiling of bovine preovulatory follicles: gonadotropin surge and prostanoid-dependent up-regulation of genes potentially linked to the ovulatory process

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