Endometrial nitric oxide production and nitric oxide synthases in the equine endometrium: Relationship with microvascular density during the estrous cycle.
Abstract: Nitric oxide (NO) plays an important role in angiogenesis and in the regulation of the blood flow. This study was carried out to investigate (i) the effects of endogenous estrogens and progestins and exogenous progesterone (P(4)) (5 ng/ml or 1 microg/ml) or estradiol 17beta (E(2)beta) (50 pg/ml or 1 microg/ml) on in vitro endometrial NO synthesis; (ii) the presence of different isoforms of NO synthase; (iii) and their relationship to microvascular density in the equine endometrium during the estrous cycle. NOS expression was also evaluated in the myometrium. Expression of endothelial and inducible forms of NOS in the uterus was assessed by Western blot and immunocytochemistry. Vascular density in endometrial tissue was determined on histologic sections. In the luteal phase, compared to the follicular phase, endometrial NO production increased without exogenous hormones and with exogenous E(2)beta (1 microg/ml). Although immunocytochemistry revealed iNOS and eNOS expression in the endometrium, no positive signal for iNOS was detected by Western blot. Endothelial NOS was observed in endometrial glands, endothelial cells, fibroblasts, blood and lymphatic vessels. Endometrial eNOS expression was the highest in the follicular and mid-luteal phases while it was found to be the lowest in the early luteal phase. In the follicular phase, hyperplasia of endometrial tissue with respect to myometrium was detected. No difference in vascular density was present between phases. All together, NO may play some roles in both proliferative and secretory phases of endometrial development in the mare.
Publication Date: 2006-04-19 PubMed ID: 16647832DOI: 10.1016/j.domaniend.2006.03.007Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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This research article focuses on the investigation of nitric oxide (NO) production and nitric oxide synthases in the equine endometrium, and their relationship with microvascular density during the estrous cycle.
Objective of Research
The research was conducted with multiple objectives. These included:
- Comprehending the effects of estrogens, progestins, progesterone, or estradiol on endometrial nitric oxide synthesis within the equine endometrium.
- Identifying the different isoforms of NO synthase present in the study subjects and their quantities.
- Establishing the connection between these quantities and the microvascular density in the endometrium during the equine estrous cycle.
Research Methodology
NOS expression was evaluated not just in the equine endometrium but also in the myometrium. Techniques like Western blot and immunocytochemistry were used to assess the expression of endothelial and inducible forms of NOS in the uterus. In order to determine the vascular density, endometrial tissue samples were checked on histologic sections.
Research Findings
The researchers found that during the luteal phase, compared to the follicular phase, endometrium’s NO production increased without the need for exogenous hormones and with exogenous estradiol. The study revealed the presence of both inducible Nitrate Oxide Synthase (iNOS) and endothelial Nitrate Oxide Synthase (eNOS) in the endometrium. However, the western blot failed to identify any signal for iNOS.
The research also concluded that eNOS was present in endometrial glands, endothelial cells, fibroblasts, as well as blood and lymphatic vessels. The highest expression of endometrial eNOS was observed in the follicular and mid-luteal phases, with the lowest expression observed in the early luteal phase.
Implications of Findings
The increase in the endometrial NO production in the luteal phase without extrinsic hormones and with E₂β (estradiol) implies that NO might play a critical role in the proliferative and secretory phases of the equine endometrial developmental cycle. The constant vascular density throughout the phases also suggests that NO might play some roles in both proliferative and secretory phases of endometrial development in the mare.
Cite This Article
APA
Roberto da Costa RP, Ferreira-Dias G, Mateus L, Korzekwa A, Andronowska A, Platek R, Skarzynski DJ.
(2006).
Endometrial nitric oxide production and nitric oxide synthases in the equine endometrium: Relationship with microvascular density during the estrous cycle.
Domest Anim Endocrinol, 32(4), 287-302.
https://doi.org/10.1016/j.domaniend.2006.03.007 Publication
Researcher Affiliations
- Escola Superior Agrária de Coimbra, Coimbra, Portugal.
MeSH Terms
- Animals
- Capillaries / metabolism
- Endometrium / blood supply
- Endometrium / growth & development
- Endometrium / metabolism
- Estradiol / physiology
- Estrous Cycle / metabolism
- Female
- Horses / physiology
- Isoenzymes
- Nitric Oxide / metabolism
- Nitric Oxide Synthase / classification
- Nitric Oxide Synthase / metabolism
Citations
This article has been cited 12 times.- Jasiński T, Zdrojkowski Ł, Ferreira-Dias G, Kautz E, Juszczuk-Kubiak E, Domino M. Molecular Mechanism of Equine Endometrosis: The NF-κB-Dependent Pathway Underlies the Ovarian Steroid Receptors' Dysfunction. Int J Mol Sci 2022 Jul 1;23(13).
- Jasiński T, Zdrojkowski Ł, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. The NF-κB-signalling pathway in mare's endometrium infiltrated with the inflammatory cells. Reprod Domest Anim 2022 Jun;57(6):598-610.
- Amaral A, Fernandes C, Szóstek-Mioduchowska A, Lukasik K, Rebordão MR, Pinto-Bravo P, Skarzynski DJ, Ferreira-Dias G. The Inhibitory Effect of Noscapine on the In Vitro Cathepsin G-Induced Collagen Expression in Equine Endometrium. Life (Basel) 2021 Oct 19;11(10).
- Rebordão MR, Amaral A, Fernandes C, Silva E, Lukasik K, Szóstek-Mioduchowska A, Pinto-Bravo P, Galvão A, Skarzynski DJ, Ferreira-Dias G. Enzymes Present in Neutrophil Extracellular Traps May Stimulate the Fibrogenic PGF(2α) Pathway in the Mare Endometrium. Animals (Basel) 2021 Sep 6;11(9).
- Amaral A, Fernandes C, Szóstek-Mioduchowska A, Rebordão MR, Skarzynski DJ, Ferreira-Dias G. Noscapine Acts as a Protease Inhibitor of In Vitro Elastase-Induced Collagen Deposition in Equine Endometrium. Int J Mol Sci 2021 May 19;22(10).
- Pinto-Bravo P, Rebordão MR, Amaral A, Fernandes C, Galvão A, Silva E, Pessa-Santos P, Alexandre-Pires G, Roberto da Costa RP, Skarzynski DJ, Ferreira-Dias G. Microvascularization and Expression of Fibroblast Growth Factor and Vascular Endothelial Growth Factor and Their Receptors in the Mare Oviduct. Animals (Basel) 2021 Apr 12;11(4).
- Amaral A, Fernandes C, Rebordão MR, Szóstek-Mioduchowska A, Lukasik K, Pinto-Bravo P, Telo da Gama L, Jan Skarzynski D, Ferreira-Dias G. Myeloperoxidase Inhibition Decreases the Expression of Collagen and Metallopeptidase in Mare Endometria under In Vitro Conditions. Animals (Basel) 2021 Jan 16;11(1).
- Alexandre-Pires G, Mateus L, Martins C, Ferreira-Dias G. Seasonal Changes in Testes Vascularisation in the Domestic Cat (Felis domesticus): Evaluation of Microvasculature, Angiogenic Activity, and Endothelial Cell Expression. Anat Res Int 2012;2012:583798.
- Kuracinova T, Bollova M, Kocan D, Mikus Kuracinova K, Janegova A, Janega P. Nitric Oxide Synthase Expression in Endometrium During Physiological Cycle. Physiol Res 2025 Dec 31;74(Suppl 2):S285-S292.
- Sadowska A, Molcan T, Słyszewska M, Skarzynski DJ, Ferreira-Dias G, Szóstek-Mioduchowska A. Transcriptomic Insights into Tumor Necrosis Factor α's Role in the Fibrosis-Related Processes of Equine Endometrial Fibroblasts. Int J Mol Sci 2025 Nov 24;26(23).
- Wydorski PJ, Zmijewska A, Franczak A. The Extremely-Low-Frequency Electromagnetic Field Affects Apoptosis and Oxidative-Stress-Related Genes and Proteins in the Porcine Endometrium-An In Vitro Study. Int J Mol Sci 2024 Jun 25;25(13).
- Zhang W, Chen SJ, Guo LY, Zhang Z, Zhang JB, Wang XM, Meng XB, Zhang MY, Zhang KK, Chen LL, Li YW, Wen Y, Wang L, Hu JH, Bai YY, Zhang XJ. Nitric oxide synthase and its function in animal reproduction: an update. Front Physiol 2023;14:1288669.
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