Leukotriene production profiles and actions in the bovine endometrium during the oestrous cycle
Anna J. Korzekwa A C , Robert Milewski B , Martyna Łupicka A and Dariusz J. Skarzynski A
+ Author Affiliations
- Author Affiliations
A Department of Reproductive Immunology and Pathology of the Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima 10 St., 10-747 Olsztyn, Poland.
B Department of Statistics and Medical Informatics, Medical University of Bialystok, Szpitalna 37 St., 15-295 Bialystok, Poland.
C Corresponding author. Email: a.korzekwa@pan.olsztyn.pl
Reproduction, Fertility and Development 28(6) 682-689 https://doi.org/10.1071/RD14301
Submitted: 17 August 2014 Accepted: 10 September 2014 Published: 13 November 2014
Abstract
We have previously shown the influence of leukotrienes (LTs) on reproductive functions in vivo: LTB4 is luteotrophic and supports corpus luteum function inducing PGE2 and progesterone (P4) secretion, whereas LTC4 is luteolytic and stimulates PGF2α secretion in cattle. The aim of this study was to examine expression and production profiles of LTs and their actions in the endometrium. LT receptors (LTB4R for LTB4 and CysLTR2 for LTC4), 5-lipoxygenase (LO), 12-LO synthase (LTCS) and LTA4 hydrolase (LTAH) mRNA and protein expression, as well as LT production were measured in bovine endometrial tissue during the luteal phases of the oestrous cycle. The action of LTs on uterine function was studied by measuring the level of PGs after stimulating uterine slices with LTs on Days 8–10 of the cycle. Expression of 5-LO and LTB4R mRNA and protein were highest on Days 2–4 of the cycle, while CysLTR2 and LTCS were highest on Days 16–18 (P < 0.05). LTB4 concentration was highest on Days 2–4 of the cycle, whereas the greatest LTC4 level was on Days 16–18 (P < 0.05). Both LTB4 and C4 increased the content of PGE2 and F2α in endometrial slices at a dose of 10–7 M (P < 0.05). In summary, mRNA expression and activation of receptors for LTB4 and production occur in the first part of the cycle, whereas LTC4 and its receptors predominate at the end of the cycle. The 12-LO and 5-LO pathways are complementary routes of LT production in the bovine uterus.
Additional keywords: arachidonic acid, cow, reproduction, uterus.
References
Barański, W., Łukasik, K., Skarżyński, D., Sztachańska, M., Zduńczyk, S., and Janowski, T. (2013). Secretion of prostaglandins and leukotrienes by endometrial cells in cows with subclinical and clinical endometritis. Theriogenology 80, 766–772.| Secretion of prostaglandins and leukotrienes by endometrial cells in cows with subclinical and clinical endometritis.Crossref | GoogleScholarGoogle Scholar | 23932172PubMed |
Blair, R. M., Saatman, R., Liou, S. S., Fortune, J. E., and Hansel, W. (1997). Roles of leukotrienes in bovine corpus luteum regression: an in vivo microdialysis study. Proc. Soc. Exp. Biol. Med. 216, 72–80.
| Roles of leukotrienes in bovine corpus luteum regression: an in vivo microdialysis study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtlOltr0%3D&md5=68314ec84ef2d8e26c403dfca24d95b9CAS | 9316613PubMed |
Bollwein, H., Meyer, H. H., Maierl, J., Weber, F., Baumgartner, U., and Stolla, R. (2000). Transrectal Doppler sonography of uterine blood flow. Theriogenology 53, 1541–1552.
| Transrectal Doppler sonography of uterine blood flow.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvislCquw%3D%3D&md5=a0580907f968c010cc88e24d61b08a9dCAS | 10883842PubMed |
Brown, N. L., Slater, D. M., Alvi, S. A., Elder, M. G., Sullivan, M. H., and Bennett, P. R. (1999). Expression of 5-lipoxygenase and 5-lipoxygenase-activating protein in human fetal membranes throughout pregnancy and at term. Mol. Hum. Reprod. 5, 668–674.
| Expression of 5-lipoxygenase and 5-lipoxygenase-activating protein in human fetal membranes throughout pregnancy and at term.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVOit7g%3D&md5=038a19cb48a2d1cbc965e92e05cbc4edCAS | 10381823PubMed |
Cerri, R. L., Chebel, R. C., Rivera, F., Narciso, C. D., Oliveira, R. A., Amstalden, M., Baez-Sandoval, G. M., Oliveira, L. J., Thatcher, W. W., and Santos, J. E. (2011). Concentration of progesterone during the development of the ovulatory follicle: II. Ovarian and uterine responses. J. Dairy Sci. 94, 3352–3365.
| Concentration of progesterone during the development of the ovulatory follicle: II. Ovarian and uterine responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFahsrg%3D&md5=b9c754c24c4b77bc0e70b259e4b0bf61CAS | 21700021PubMed |
Cerri, R. L., Thompson, I. M., Kim, I. H., Ealy, A. D., Hansen, P. J., Staples, C. R., Li, J. L., Santos, J. E., and Thatcher, W. W. (2012). Effects of lactation and pregnancy on gene expression of endometrium of Holstein cows at Day 17 of the oestrous cycle or pregnancy. J. Dairy Sci. 95, 5657–5675.
| Effects of lactation and pregnancy on gene expression of endometrium of Holstein cows at Day 17 of the oestrous cycle or pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVCns7rJ&md5=841fc15d4fad2f3222c1bd7750b8aa2eCAS | 22884349PubMed |
Ciereszko, R., Opałka, M., Kamińska, B., Wojtczak, M., Okrasa, S., and Dusza, L. (2001). Luteotrophic action of prolactin during the early luteal phase in pigs: the involvement of protein kinases and phosphatases. Reprod. Biol. 1, 62–83.
| 1:STN:280:DC%2BD3srosFWrsA%3D%3D&md5=6ee4e05466642302e3bea4a5a8a785c5CAS | 14666168PubMed |
Corriveau, S., Rousseau, E., Berthiaume, M., and Pasquier, J. C. (2010). Lipoxygenase and cyclooxygenase inhibitors reveal a complementary role of arachidonic acid derivatives in pregnant human myometrium. Am. J. Obstet. Gynecol. 203, 266.e1–266.e7.
| Lipoxygenase and cyclooxygenase inhibitors reveal a complementary role of arachidonic acid derivatives in pregnant human myometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWqtL%2FJ&md5=35ab499fb9d99779265aa393712f7ffcCAS |
Eaton, A., Nagy, E., Pacault, M., Fauconnier, J., and Bäck, M. (2012). Cysteinyl leukotriene signalling through perinuclear CysLT(1) receptors on vascular smooth muscle cells transduces nuclear calcium signalling and alterations of gene expression. J. Mol. Med. (Berl) 90, 1223–1231.
| Cysteinyl leukotriene signalling through perinuclear CysLT(1) receptors on vascular smooth muscle cells transduces nuclear calcium signalling and alterations of gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlGhsbrP&md5=2a7917b8ad7ea7bda011410809a1879fCAS | 22527886PubMed |
Izumi, T., Yokomizo, T., Obinata, H., Ogasawara, H., and Shimizu, T. (2002). Leukotriene receptors: classification, gene expression and signal transduction. J. Biochem. 132, 1–6.
| Leukotriene receptors: classification, gene expression and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslCitbo%3D&md5=845fea9c610d615d46ba382c0d25befeCAS | 12097153PubMed |
Jones, T. R., and Rodger, I. W. (1999). Role of leukotrienes and leukotriene receptor antagonists in asthma. Pulm. Pharmacol. Ther. 12, 107–110.
| Role of leukotrienes and leukotriene receptor antagonists in asthma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVOntLw%3D&md5=090d40bf9b6b2c8b514c3488241ad640CAS | 10373391PubMed |
Kamohara, M., Takasaki, J., Matsumoto, M., Matsumoto, S., Saito, T., Soga, T., Matsushime, H., and Furuichi, K. (2001). Functional characterization of cysteinyl leukotriene CysLT(2) receptor on human coronary artery smooth-muscle cells. Biochem. Biophys. Res. Commun. 287, 1088–1092.
| Functional characterization of cysteinyl leukotriene CysLT(2) receptor on human coronary artery smooth-muscle cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnt1Oktr8%3D&md5=8702e2f6fec4e9c4dbf88b13aa45ad52CAS | 11587533PubMed |
Korzekwa, A., Murakami, S., Wocławek-Potocka, I., Bah, M. M., Okuda, K., and Skarzynski, D. J. (2008). The influence of tumour necrosis factor alpha (TNF) on the secretory function of bovine corpus luteum: TNF and its receptors expression during the oestrous cycle. Reprod. Biol. 8, 245–262.
| The influence of tumour necrosis factor alpha (TNF) on the secretory function of bovine corpus luteum: TNF and its receptors expression during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 19092986PubMed |
Korzekwa, A. J., Bah, M. M., Kurzynowski, A., Lukasik, K., Groblewska, A., and Skarzynski, D. J. (2010a). Leukotrienes modulate secretion of progesterone and prostaglandins during the oestrous cycle and early pregnancy in cattle: an in vivo study. Reproduction 140, 767–776.
| Leukotrienes modulate secretion of progesterone and prostaglandins during the oestrous cycle and early pregnancy in cattle: an in vivo study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCntr7P&md5=8d8c689b118b13a30263d046665a51a3CAS | 20813877PubMed |
Korzekwa, A. J., Acosta, T. J., Miklewicz, M., Lee, S. H., and Skarzynski, D. J. (2010b). Leukotrienes affect secretory function of ovarian cells in vitro. Reprod. Domest. Anim. 45, e288–e296.
| Leukotrienes affect secretory function of ovarian cells in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLnE&md5=ac74173f7bebeec52438ea7c6e1e21b0CAS | 20002606PubMed |
Korzekwa, A., Lukasik, K., and Skarzynski, D. J. (2010c). Leukotrienes are auto-/paracrine factors in the bovine corpus luteum: an in vitro study. Reprod. Domest. Anim. 45, 1089–1097.
| Leukotrienes are auto-/paracrine factors in the bovine corpus luteum: an in vitro study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1WrsLjF&md5=29cde68a25478f1efaa20fa69c76ab57CAS | 19645858PubMed |
Korzekwa, A. J., Bodek, G., Bukowska, J., Blitek, A., and Skarzynski, D. J. (2011). Characterization of bovine immortalized luteal endothelial cells: action of cytokines on production and content of arachidonic acid metabolites. Reprod. Biol. Endocrinol. 9, 27.
| Characterization of bovine immortalized luteal endothelial cells: action of cytokines on production and content of arachidonic acid metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtl2murw%3D&md5=c8fde7b7e4ddb72f908204399e4d5f64CAS | 21349168PubMed |
Kühn, H., and O’Donnell, V. B. (2006). Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 45, 334–356.
| Inflammation and immune regulation by 12/15-lipoxygenases.Crossref | GoogleScholarGoogle Scholar | 16678271PubMed |
McCracken, J. A., Custer, E. E., and Lamsa, J. C. (1999). Luteolysis: a neuroendocrine-mediated event. Physiol. Rev. 79, 263–323.
| 1:CAS:528:DyaK1MXivFektLg%3D&md5=074c6537a7115feb0591a1e2a4d8bb8fCAS | 10221982PubMed |
Milvae, R. A., Alila, H. W., and Hansel, W. (1986). Involvement of lipoxygenase products of arachidonic acid metabolism in bovine luteal function. Biol. Reprod. 35, 1210–1215.
| Involvement of lipoxygenase products of arachidonic acid metabolism in bovine luteal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtFCitLg%3D&md5=5a6d53d0a94d562170a662f11490e98fCAS | 3103701PubMed |
Miyamoto, Y., Skarzynski, D. J., and Okuda, K. (2000). Is tumour necrosis factor-α a trigger for the initiation of prostaglandin F2α release at luteolysis in cattle? Biol. Reprod. 62, 1109–1115.
| Is tumour necrosis factor-α a trigger for the initiation of prostaglandin F2α release at luteolysis in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2htr8%3D&md5=4109fe57528feee511845fc94598cb5eCAS | 10775155PubMed |
Molin, D. G., van den Akker, N. M., and Post, M. J. (2010). ‘Lox on neovascularisation’: leukotrienes as mediators in endothelial biology. Cardiovasc. Res. 86, 6–8.
| ‘Lox on neovascularisation’: leukotrienes as mediators in endothelial biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1GitLk%3D&md5=45cbce176f9fc1414a0152524b35cec0CAS | 20181674PubMed |
Murphy, R. C., and Gijón, M. A. (2007). Biosynthesis and metabolism of leukotrienes. Biochem. J. 405, 379–395.
| Biosynthesis and metabolism of leukotrienes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns12gsr4%3D&md5=8e26762e2d6fa185bf902333579692daCAS | 17623009PubMed |
Padma, A. S., Agarwal, S., Reddy, D. B., Prasad, T. S., and Reddanna, P. (2007). Metabolism of arachidonic acid in sheep uterus: in vitro studies. Indian J. Biochem. Biophys. 44, 216–222.
| 1:CAS:528:DC%2BD2sXht1KmsrvI&md5=db886be16dc6627828027ece606bccaaCAS | 17970279PubMed |
Samuelsson, B. (2000). The discovery of the leukotrienes. Am. J. Respir. Crit. Care Med. 161, S2–S6.
| The discovery of the leukotrienes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7otVartQ%3D%3D&md5=47f760c15a58d95764a572748a56d013CAS | 10673217PubMed |
Sheldon, I. M., Cronin, J., Goetze, L., Donofrio, G., and Schuberth, H. J. (2009). Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol. Reprod. 81, 1025–1032.
| Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2lt7vP&md5=e5e17407d4dc225c4858153d0ee78eb4CAS | 19439727PubMed |
Singh, R. K., Gupta, S., Dastidar, S., and Ray, A. (2010). Cysteinyl leukotrienes and their receptors: molecular and functional characteristics. Pharmacology 85, 336–349.
| Cysteinyl leukotrienes and their receptors: molecular and functional characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosFart7o%3D&md5=28f9ad486050658d78b07fa57f9e8f4fCAS | 20516735PubMed |
Skarzynski, D. J., Bah, M. M., Deptula, K. M., Woclawek-Potocka, I., Korzekwa, A., Shibaya, M., Pilawski, W., and Okuda, K. (2003). Roles of tumour necrosis factor-alpha of the oestrous cycle in cattle: an in vivo study. Biol. Reprod. 69, 1907–1913.
| Roles of tumour necrosis factor-alpha of the oestrous cycle in cattle: an in vivo study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVCns7Y%3D&md5=c26e6eb39a2ee8caf7db4280871d883cCAS | 12904309PubMed |
Slama, H., Vaillancourt, D., and Goff, A. K. (1993). Leukotriene B4 in cows with normal calving, and in cows with retained fetal membranes and/or uterine subinvolution. Can. J. Vet. Res. 57, 293–299.
| 1:CAS:528:DyaK2cXhsFClu7w%3D&md5=e85c69662593f6d0ec4a19f5ade92fe7CAS | 8269369PubMed |
Tager, A. M., and Luster, A. D. (2003). BLT1 and BLT2: the leukotriene B4 receptors. Prostaglandins Leukot. Essent. Fatty Acids 69, 123–134.
| BLT1 and BLT2: the leukotriene B4 receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVKjsbw%3D&md5=ae23509ddbdfad9a3e835fd1084f65d9CAS | 12895595PubMed |
Uenoyama, Y., Hattori, S., Miyake, M., and Okuda, K. (1997). Up-regulation of oxytocin receptors in porcine endometrium by adenosine 3′,5′-monophosphate. Biol. Reprod. 57, 723–728.
| Up-regulation of oxytocin receptors in porcine endometrium by adenosine 3′,5′-monophosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtFCqsrk%3D&md5=da128e664d378ba1ca7ebf9d9821a474CAS | 9314572PubMed |
Weems, C. W., Weems, Y. S., and Randel, R. D. (2006). Prostaglandins and reproduction in female farm animals. Vet. J. 171, 206–228.
| Prostaglandins and reproduction in female farm animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsF2ntLo%3D&md5=31dc37638a76ac9cc80e5719bc0f066dCAS | 16490704PubMed |
