Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor

Dickson, S. E.; Bicknell, Roy; Fraser, H. M.

doi:10.1677/joe.0.1680409

Cited by 71 publications

(36 citation statements)

References 22 publications

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“…Inhibition of LH signalling using GNRH antagonists mimicked this effect, also suppressing early luteal angiogenesis and implicating the LH surge in normal luteal angiogenesis, consistent with the described induction of VEGFA signalling by LH (Koos 1995, Dickson & Fraser 2000. The in vivo inhibition of VEGFA signalling throughout the luteal phase (days 3-10 in the marmoset monkey) also decreased luteal angiogenesis and the blood concentration of progesterone (Dickson et al 2001, Wulff et al 2001c. Recently, a study carried out by Christensen et al (2012) indicated that treatment with progesterone increased the levels of VEGFA, KDR and angiopoietin 1 (ANGPT1 (ANG1)) in the CL of anoestrous ewes.…”

Section: Discussionsupporting

confidence: 71%

Short oestrous cycles in sheep during anoestrus involve defects in progesterone biosynthesis and luteal neovascularisation

Brown

Nys²,

Cognié³

et al. 2014

Reproduction

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Anoestrous ewes can be induced to ovulate by the socio-sexual, 'ram effect'. However, in some ewes, the induced ovulation is followed by an abnormally short luteal phase causing a so-called 'short cycle'. The defect responsible for this luteal dysfunction has not been identified. In this study, we investigated ovarian and uterine factors implicated in male-induced short cycles in anoestrous ewes using a combined endocrine and molecular strategy. Before ovulation, we were able to detect a moderate loss of thecal expression of steroid acute regulatory protein (STAR) in ewes that had not received progesterone priming (which prevents short cycles). At and following ovulation, we were able to identify a significant loss of expression of genes coding key proteins involved in the biosynthesis of progesterone (STAR, CYP11A1 and HSD3B1 (HSD3B)) as well as genes coding proteins critical for vascular development during early luteal development (VEGFA and KDR (VEGFR2)), suggesting dysfunction in at least two pathways critical for normal luteal function. Furthermore, these changes were associated with a significant reduction of progesterone production and luteal weight. Additionally, we cast doubt on the proposed uterus-mediated effect of prostaglandin F2a (PGF2a) as a cause of short cycles by demonstrating the dysregulation of luteal expression of the PGF receptor, which mediates the luteal effects of PGF2a, and by finding no significant changes in the circulating concentrations of PGFM, the principal metabolite of PGF2a in ewes with short cycles. This study is the first of its kind to examine concurrently the endocrine and molecular events in the follicular and early luteal stages of the short cycle. Free French abstractA French translation of this abstract is freely available at

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Section: Discussionsupporting

confidence: 71%

Short oestrous cycles in sheep during anoestrus involve defects in progesterone biosynthesis and luteal neovascularisation

Brown

Nys²,

Cognié³

et al. 2014

Reproduction

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“…Indeed, endothelial cells may be particularly sensitive to the loss of growth factor support during tubule initiation. A requirement for positive survival signals in luteal development has been suggested (Hojo et al 2010) and apoptotic endothelial cells have been localised in primate corpora lutea following VEGFA-suppression (Dickson et al 2001). In addition, the FGF2-independence that develops over time in culture in this study may reflect an increasing resistance to endothelial cell apoptosis that occurs as vessel-like structures mature and recruit perivascular cells (Benjamin et al 1998(Benjamin et al , 1999.…”

Section: Fgf2 and Luteal Endothelial Cell Sproutingmentioning

confidence: 66%

Fibroblast growth factor 2 is a key determinant of vascular sprouting during bovine luteal angiogenesis

Woad¹,

Hunter²,

Mann³

et al. 2012

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Fibroblast growth factor (FGF) 2 and vascular endothelial growth factor (VEGF) A are thought to be key controllers of luteal angiogenesis; however, their precise roles in the regulation and coordination of this complex process remain unknown. Thus, the temporal and spatial patterns of endothelial network formation were determined by culturing mixed cell types from early bovine corpora lutea on fibronectin in the presence of FGF2 and VEGFA (6 h to 9 days). Endothelial cells, as determined by von Willebrand factor immunohistochemistry, initially grew in cell islands (days 0-3), before undergoing a period of vascular sprouting to display a more tubule-like appearance (days 3-6), and after 9 days in culture had formed extensive intricate networks. Mixed populations of luteal cells were treated with SU1498 (VEGF receptor 2 inhibitor) or SU5402 (FGF receptor 1 inhibitor) or control on days 0-3, 3-6 or 6-9 to determine the role of FGF2 and VEGFA during these specific windows. The total area of endothelial cells was unaffected by SU1498 treatment during any window. In contrast, SU5402 treatment caused maximal reduction in the total area of endothelial cell networks on days 3-6 vs controls (mean reduction 81%; P!0.001) during the period of tubule initiation. Moreover, SU5402 treatment on days 3-6 dramatically reduced the total number of branch points (P!0.001) and degree of branching per endothelial cell island (P!0.05) in the absence of changes in mean island area. This suggests that FGF2 is a key determinant of vascular sprouting and hence critical to luteal development.

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“…However, endothelial cells are also among the first cells to undergo apoptosis, or "angioregression" during regression of the CL [8]. There is general agreement that a surge of angiogenesis occurs within the CL during its initial development, which is characterized by increased proliferation of endothelial cells and secretion of vascular endothelial cell growth factor (VEGF), and the upregulation of angiopoetins [9][10][11][12][13][14][15]. There is discrepancy, however, about whether or not a second surge of angiogenesis occurs during early pregnancy [9,11,13,16].…”

mentioning

confidence: 99%

Microvascular Endothelial Cells of the Bovine Corpus Luteum: A Comparative Examination of the Estrous Cycle and Pregnancy

Cherry

Hou

Rueda

et al. 2008

Journal of Reproduction and Development

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Abstract. Endothelial cells derived from the corpus luteum (CLENDOs) exhibit diverse characteristics presumably serving their wide-ranging roles in luteal function and fate. Here, several attributes of CLENDOs derived from cows at midcycle (days 9-12 of the estrous cycle) were compared with CLENDOs from early pregnancy (day 60 of pregnancy). Flow cytometric analysis of cells fluorescently-tagged with the lectins Bandeiraea simplicifolia (BS-1) and Concanavalin A (ConA) indicated that CLENDOs of midcycle CL do not differ from those of pregnancy. Mean fluorescence intensity for BS-1 was 15 ± 1 and 23 ± 7 fluorescent units for midcycle CLENDOs and CLENDOs of pregnancy, respectively (P>0.05). For ConA, mean fluorescence was 25 ± 2 and 26 ± 1 fluorescent units, respectively (P>0.05). The CLENDOs were also exposed to cytokines to assess differences in activation of nuclear factor kappa B signaling (NF-κB), induction of the transcription factor interferon regulatory factor 1 (IRF1), cytokine production, and cytokine-induced cell death. In response to TNF, for instance, both types of CLENDOs exhibited a rapid, 5-fold decrease in NF-κB inhibitor alpha (NFKBIA) protein expression (P<0.05), and a 4-fold increase in IRF1 expression (P<0.05), that did not differ with phenotype (P>0.05). Similarly, both types of CLENDOs produced tumor necrosis factor alpha and chemokine ligand 2 in response to IFNG stimulation (P<0.05) that did not differ with phenotype (P>0.05). Lastly, extended exposure of CLENDOs of midcycle CL to cytokines induced cell death (~50% cell death vs. control) similar to the incidence of cell death seen previously in CLENDOs of early pregnancy. The results indicate that several physical and functional characteristics of CLENDOs of midcycle CL are retained through early pregnancy, including lectin-binding properties, sensitivity to cytokines, and the activation of cytokine-initiated intracellular signals. Key words: Bovine, Corpus luteum, Cytokine, Endothelial cell, Lectin (J. Reprod. Dev. 54: [183][184][185][186][187][188][189][190][191] 2008) he corpus luteum (CL) is a temporary endocrine gland that forms within the ovary following ovulation and contributes to estrous/menstrual cycle regularity and the establishment of early pregnancy [1]. Aside from its transient nature, an intriguing aspect of the CL is its adaptable lifespan. In domestic livestock, the CL remains functional for as few as 15-18 days to as many as 200-300 days depending upon species and reproductive status of the animal [2]. In the cow, the CL develops, functions, and begins to regress within 17-18 days of ovulation during the estrous cycle, but retains a functional lifespan of more than 200 days during pregnancy [3] . Similarly, luteal lifespan in the ewe ranges from 15-16 days during the estrous cycle to more than 50 days during pregnancy [4]. In fact in most placental mammals the continuation of luteal function associated with pregnancy extends well beyond the period of a single estrous or menstrual cycle and is required for the establi...

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Mid-luteal angiogenesis and function in the primate is dependent on vascular endothelial growth factor

Cited by 71 publications

References 22 publications

Short oestrous cycles in sheep during anoestrus involve defects in progesterone biosynthesis and luteal neovascularisation

Short oestrous cycles in sheep during anoestrus involve defects in progesterone biosynthesis and luteal neovascularisation

Fibroblast growth factor 2 is a key determinant of vascular sprouting during bovine luteal angiogenesis

Microvascular Endothelial Cells of the Bovine Corpus Luteum: A Comparative Examination of the Estrous Cycle and Pregnancy

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