The melatonin system is expressed in the ovine uterus: effect of the day of the oestrous cycle and undernutrition
C. Sosa
A * , E. Laurenzana A , V. de Brun B , A. Meikle B and J. A. Abecia C
+ Author Affiliations
- Author Affiliations
A Departamento de Bioquímica y Biología Molecular y Celular, Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
B Laboratorio de Endocrinología y Metabolismo Animal, Facultad de Veterinaria, UdelaR, Montevideo, Uruguay.
C Instituto de Investigación en Ciencias Ambientales (IUCA), Universidad de Zaragoza, Facultad de Veterinaria, Zaragoza, Spain.
Reproduction, Fertility and Development 35(11) 563-574 https://doi.org/10.1071/RD22194
Published online: 9 June 2023
© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Melatonin influences female reproduction, but expression of the melatonin system has not been characterised in the ovine uterus.
Aims: We aimed to determine whether synthesising enzymes (arylalkylamine N-acetyltransferase (AANAT) and N-acetylserotonin-O-methyltransferase (ASMT)), melatonin receptors 1 and 2 (MT1 and MT2), and catabolising enzymes (myeloperoxidase (MPO) and indoleamine 2,3-dioxygenase 1 and 2 (IDO1 and 2)), are expressed in the ovine uterus, and if they are influenced by the oestrous cycle (Experiment 1) or by undernutrition (Experiment 2).
Methods: In Experiment 1, gene and protein expression was determined in sheep endometrium samples collected on days 0 (oestrus), 5, 10 and 14 of the oestrous cycle. In Experiment 2, we studied uterine samples from ewes fed either 1.5 or 0.5 times their maintenance requirements.
Key results: We have demonstrated the expression of AANAT and ASMT in the endometrium of sheep. AANAT and ASMT transcripts, and AANAT protein were more elevated at day 10, then decreased to day 14. A similar pattern was observed for MT2, IDO1, and MPO mRNA, which suggests that the endometrial melatonin system might be influenced by ovarian steroid hormones. Undernutrition increased AANAT mRNA expression, but seemed to decrease its protein expression, and increased MT2 and IDO2 transcripts, whereas ASMT expression was unaffected.
Conclusions: The melatonin system is expressed in the ovine uterus and is affected by oestrous cycle and undernutrition.
Implications: The results help explain the adverse effects of undernutrition on reproduction in sheep, and the success of exogenous melatonin treatments in improving reproductive outcomes.
Keywords: AANAT, ASMT, IDO, melatonin, melatonin receptor, MPO, sheep, undernutrition, uterus.
References
Abecia, JA, Forcada, F, and Zúñiga, O (2002). The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro. Veterinary Research Communications 26, 151–158.| The effect of melatonin on the secretion of progesterone in sheep and on the development of ovine embryos in vitro.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Forcada, F, Valares, JA, Zúñiga, O, and Kindahl, H (2003). Effect of exogenous melatonin on in vivo and in vitro prostaglandin secretion in Rasa Aragonesa ewes. Theriogenology 60, 1345–1355.
| Effect of exogenous melatonin on in vivo and in vitro prostaglandin secretion in Rasa Aragonesa ewes.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Sosa, C, Forcada, F, and Meikle, A (2006). The effect of undernutrition on the establishment of pregnancy in the ewe. Reproduction Nutrition Development 46, 367–378.
| The effect of undernutrition on the establishment of pregnancy in the ewe.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Forcada, F, Casao, A, and Palacín, I (2008). Effect of exogenous melatonin on the ovary, the embryo and the establishment of pregnancy in sheep. Animal 2, 399–404.
| Effect of exogenous melatonin on the ovary, the embryo and the establishment of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Forcada, F, Vázquez, M-I, Muiño-Blanco, T, Cebrián-Pérez, JA, Pérez-Pe, R, and Casao, A (2019). Role of melatonin on embryo viability in sheep. Reproduction, Fertility and Development 31, 82–92.
| Role of melatonin on embryo viability in sheep.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Garrido, C, Gave, M, García, A-I, López, D, Luis, S, Valares, JA, and Mata, L (2020a). Exogenous melatonin and male foetuses improve the quality of sheep colostrum. Journal of Animal Physiology and Animal Nutrition 104, 1305–1309.
| Exogenous melatonin and male foetuses improve the quality of sheep colostrum.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Mura, MC, Carvajal-Serna, M, Pulinas, L, Macías, A, Casao, A, Pérez-Pe, R, and Carcangiu, V (2020b). Polymorphisms of the melatonin receptor 1A (MTNR1A) gene influence the age at first mating in autumn-born ram-lambs and sexual activity of adult rams in spring. Theriogenology 157, 42–47.
| Polymorphisms of the melatonin receptor 1A (MTNR1A) gene influence the age at first mating in autumn-born ram-lambs and sexual activity of adult rams in spring.Crossref | GoogleScholarGoogle Scholar |
Abecia, JA, Luis, S, and Canto, F (2021). Implanting melatonin at lambing enhances lamb growth and maintains high fat content in milk. Veterinary Research Communications 45, 181–188.
| Implanting melatonin at lambing enhances lamb growth and maintains high fat content in milk.Crossref | GoogleScholarGoogle Scholar |
Acuña-Castroviejo, D, Escames, G, Venegas, C, Díaz-Casado, ME, Lima-Cabello, E, López, LC, Rosales-Corral, S, Tan, DX, and Reiter, RJ (2014). Extrapineal melatonin: sources, regulation, and potential functions. Cellular and Molecular Life Sciences 71, 2997–3025.
| Extrapineal melatonin: sources, regulation, and potential functions.Crossref | GoogleScholarGoogle Scholar |
Alderman G, Cottrill BR (1993) ‘Energy and protein requirements of ruminants: an advisory manual prepared by the AFRC Technical Committee on Responses to Nutrients.’ (CAB International: Wallingford, UK)
Bae, H, Yang, C, Lee, JY, Park, S, Bazer, FW, Song, G, and Lim, W (2020). Melatonin improves uterine-conceptus interaction via regulation of SIRT1 during early pregnancy. Journal of Pineal Research 69, e12670.
| Melatonin improves uterine-conceptus interaction via regulation of SIRT1 during early pregnancy.Crossref | GoogleScholarGoogle Scholar |
Carcangiu, V, Mura, MC, Vacca, GM, Pazzola, M, Dettori, ML, Luridiana, S, and Bini, PP (2009). Polymorphism of the melatonin receptor MT1 gene and its relationship with seasonal reproductive activity in the Sarda sheep breed. Animal Reproduction Science 116, 65–72.
| Polymorphism of the melatonin receptor MT1 gene and its relationship with seasonal reproductive activity in the Sarda sheep breed.Crossref | GoogleScholarGoogle Scholar |
Cardinali, DP, Nagle, CA, and Rosner, JM (1974). Effects of estradiol on melatonin and protein synthesis in the rat pineal organ. Hormone Research 5, 304–310.
| Effects of estradiol on melatonin and protein synthesis in the rat pineal organ.Crossref | GoogleScholarGoogle Scholar |
Carlomagno, G, Minini, M, Tilotta, M, and Unfer, V (2018). From implantation to birth: Insight into molecular melatonin functions. International Journal of Molecular Sciences 19, 2802.
| From implantation to birth: Insight into molecular melatonin functions.Crossref | GoogleScholarGoogle Scholar |
Casao, A, Pérez-Pé, R, Cebrián-Pérez, JA, Muiño-Blanco, T, Forcada, F, and Abecia, JA (2019). 125 Presence of melatonin receptors in ovine blastocysts. Reproduction, Fertility and Development 31, 188.
| 125 Presence of melatonin receptors in ovine blastocysts.Crossref | GoogleScholarGoogle Scholar |
Cipolla-Neto, J, Amaral, FG, Soares, JM, Congentino Gallo, C, Furtado, A, Cavaco, JE, Gonçalves, I, Santos, CRA, and Quintela, T (2022). The crosstalk between melatonin and sex steroid hormones. Neuroendocrinology 112, 115–129.
| The crosstalk between melatonin and sex steroid hormones.Crossref | GoogleScholarGoogle Scholar |
Cui, L, Xu, F, Wang, S, Jiang, Z, Liu, L, Ding, Y, Sun, X, and Du, M (2021). Melatonin-MT1 signal is essential for endometrial decidualization. Reproduction 162, 161–170.
| Melatonin-MT1 signal is essential for endometrial decidualization.Crossref | GoogleScholarGoogle Scholar |
de Brun, V, Loor, JJ, Naya, H, Graña-Baumgartner, A, Vailati-Riboni, M, Bulgari, O, Shahzad, K, Abecia, JA, Sosa, C, and Meikle, A (2021). The presence of an embryo affects day 14 uterine transcriptome depending on the nutritional status in sheep. b. Immune system and uterine remodeling. Theriogenology 161, 210–218.
| The presence of an embryo affects day 14 uterine transcriptome depending on the nutritional status in sheep. b. Immune system and uterine remodeling.Crossref | GoogleScholarGoogle Scholar |
Dubocovich, ML, and Markowska, M (2005). Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 27, 101–110.
| Functional MT1 and MT2 melatonin receptors in mammals.Crossref | GoogleScholarGoogle Scholar |
Dubocovich, ML, Delagrange, P, Krause, DN, Sugden, D, Cardinali, DP, and Olcese, J (2010). International union of basic and clinical pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors. Pharmacological Reviews 62, 343–380.
| International union of basic and clinical pharmacology. LXXV. Nomenclature, classification, and pharmacology of G protein-coupled melatonin receptors.Crossref | GoogleScholarGoogle Scholar |
Fatokun, AA, Hunt, NH, and Ball, HJ (2013). Indoleamine 2,3-dioxygenase 2 (IDO2) and the kynurenine pathway: characteristics and potential roles in health and disease. Amino Acids 45, 1319–1329.
| Indoleamine 2,3-dioxygenase 2 (IDO2) and the kynurenine pathway: characteristics and potential roles in health and disease.Crossref | GoogleScholarGoogle Scholar |
Ferry, G, Ubeaud, C, Lambert, P-H, Bertin, S, Cogé, F, Chomarat, P, Delagrange, P, Serkiz, B, Bouchet, J-P, Truscott, RJW, and Boutin, JA (2005). Molecular evidence that melatonin is enzymatically oxidized in a different manner than tryptophan: investigations with both indoleamine 2,3-dioxygenase and myeloperoxidase. Biochemical Journal 388, 205–215.
| Molecular evidence that melatonin is enzymatically oxidized in a different manner than tryptophan: investigations with both indoleamine 2,3-dioxygenase and myeloperoxidase.Crossref | GoogleScholarGoogle Scholar |
Forcada, F, Abecia, JA, Casao, A, Cebrián-Pérez, JA, Muiño-Blanco, T, and Palacín, I (2007). Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in ewes during anestrus and the reproductive season. Theriogenology 67, 855–862.
| Effects of ageing and exogenous melatonin on pituitary responsiveness to GnRH in ewes during anestrus and the reproductive season.Crossref | GoogleScholarGoogle Scholar |
Ganguly, S, Coon, SL, and Klein, DC (2002). Control of melatonin synthesis in the mammalian pineal gland: the critical role of serotonin acetylation. Cell and Tissue Research 309, 127–137.
| Control of melatonin synthesis in the mammalian pineal gland: the critical role of serotonin acetylation.Crossref | GoogleScholarGoogle Scholar |
Gonzalez-Arto, M, Hamilton, TRdS, Gallego, M, Gaspar-Torrubia, E, Aguilar, D, Serrano-Blesa, E, Abecia, JA, Pérez-Pé, R, Muiño-Blanco, T, Cebrián-Pérez, JA, and Casao, A (2016). Evidence of melatonin synthesis in the ram reproductive tract. Andrology 4, 163–171.
| Evidence of melatonin synthesis in the ram reproductive tract.Crossref | GoogleScholarGoogle Scholar |
He, C, Wang, J, Li, Y, Zhu, K, Xu, Z, Song, Y, Song, Y, and Liu, G (2015). Melatonin-related genes expressed in the mouse uterus during early gestation promote embryo implantation. Journal of Pineal Research 58, 300–309.
| Melatonin-related genes expressed in the mouse uterus during early gestation promote embryo implantation.Crossref | GoogleScholarGoogle Scholar |
Hernández-Díaz, FJ, Sánchez, JJ, Abreu, P, López-Coviella, I, Tabares, L, Prieto, L, and Alonso, R (2001). Estrogen modulates α1/β-adrenoceptor-induced signaling and melatonin production in female rat pinealocytes. Neuroendocrinology 73, 111–122.
| Estrogen modulates α1/β-adrenoceptor-induced signaling and melatonin production in female rat pinealocytes.Crossref | GoogleScholarGoogle Scholar |
Hu, J-J, Xiao, L-F, Song, L-L, Ge, W-B, Duan, H-W, and Jiang, Y (2020). The expression of melatonin receptors MT1 and MT2 is regulated by E2 in sheep oviduct. General and Comparative Endocrinology 286, 113135.
| The expression of melatonin receptors MT1 and MT2 is regulated by E2 in sheep oviduct.Crossref | GoogleScholarGoogle Scholar |
Itoh, MT, Ishizuka, B, Kudo, Y, Fusama, S, Amemiya, A, and Sumi, Y (1997). Detection of melatonin and serotonin N-acetyltransferase and hydroxyindole-O-methyltransferase activities in rat ovary. Molecular and Cellular Endocrinology 136, 7–13.
| Detection of melatonin and serotonin N-acetyltransferase and hydroxyindole-O-methyltransferase activities in rat ovary.Crossref | GoogleScholarGoogle Scholar |
Itoh, MT, Ishizuka, B, Kuribayashi, Y, Amemiya, A, and Sumi, Y (1999). Melatonin, its precursors, and synthesizing enzyme activities in the human ovary. Molecular Human Reproduction 5, 402–408.
| Melatonin, its precursors, and synthesizing enzyme activities in the human ovary.Crossref | GoogleScholarGoogle Scholar |
Ivanov, D, Mazzoccoli, G, Anderson, G, Linkova, N, Dyatlova, A, Mironova, E, Polyakova, V, Kvetnoy, I, Evsyukova, I, Carbone, A, and Nasyrov, R (2021). Melatonin, its beneficial effects on embryogenesis from mitigating oxidative stress to regulating gene expression. International Journal of Molecular Sciences 22, 5885.
| Melatonin, its beneficial effects on embryogenesis from mitigating oxidative stress to regulating gene expression.Crossref | GoogleScholarGoogle Scholar |
Iwasaki, S, Nakazawa, K, Sakai, J, Kometani, K, Iwashita, M, Yoshimura, Y, and Maruyama, T (2005). Melatonin as a local regulator of human placental function. Journal of Pineal Research 39, 261–265.
| Melatonin as a local regulator of human placental function.Crossref | GoogleScholarGoogle Scholar |
Jockers, R, Delagrange, P, Dubocovich, ML, Markus, RP, Renault, N, Tosini, G, Cecon, E, and Zlotos, DP (2016). Update on melatonin receptors: IUPHAR Review 20. British Journal of Pharmacology 173, 2702–2725.
| Update on melatonin receptors: IUPHAR Review 20.Crossref | GoogleScholarGoogle Scholar |
Li, D-D, Liu, X-Y, Guo, C-H, Yue, L, Yang, Z-Q, Cao, H, Guo, B, and Yue, Z-P (2015). Differential expression and regulation of Ido2 in the mouse uterus during peri-implantation period. In Vitro Cellular & Developmental Biology – Animal 51, 264–272.
| Differential expression and regulation of Ido2 in the mouse uterus during peri-implantation period.Crossref | GoogleScholarGoogle Scholar |
Livak, KJ, and Schmittgen, TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method.Crossref | GoogleScholarGoogle Scholar |
Martínez-Marcos, P, Carvajal-Serna, M, Lázaro-Gaspar, S, Pérez-Pé, R, Muiño-Blanco, T, Cebrián-Pérez, JA, and Casao, A (2019). Presence of melatonin-catabolizing non-specific enzymes myeloperoxidase and indoleamine 2,3-dioxygenase in the ram reproductive tract. Reproduction in Domestic Animals 54, 1643–1650.
| Presence of melatonin-catabolizing non-specific enzymes myeloperoxidase and indoleamine 2,3-dioxygenase in the ram reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Meikle, A, de Brun, V, Carriquiry, M, Soca, P, Sosa, C, Adrien, ML, Chilibroste, P, and Abecia, JA (2018). Influences of nutrition and metabolism on reproduction of the female ruminant. Animal Reproduction 15, 899–911.
| Influences of nutrition and metabolism on reproduction of the female ruminant.Crossref | GoogleScholarGoogle Scholar |
Mellor, AL, Chandler, P, Lee, GK, Johnson, T, Keskin, DB, Lee, J, and Munn, DH (2002). Indoleamine 2,3-dioxygenase, immunosuppression and pregnancy. Journal of Reproductive Immunology 57, 143–150.
| Indoleamine 2,3-dioxygenase, immunosuppression and pregnancy.Crossref | GoogleScholarGoogle Scholar |
Merlo, LMF, and Mandik-Nayak, L (2016). IDO2: a pathogenic mediator of inflammatory autoimmunity. Clinical Medicine Insights: Pathology 9s1, CPath.S39930.
| IDO2: a pathogenic mediator of inflammatory autoimmunity.Crossref | GoogleScholarGoogle Scholar |
Merlo, LMF, Peng, W, and Mandik-Nayak, L (2022). Impact of IDO1 and IDO2 on the B cell immune response. Frontiers in Immunology 13, 886225.
| Impact of IDO1 and IDO2 on the B cell immune response.Crossref | GoogleScholarGoogle Scholar |
Mosher, AA, Tsoulis, MW, Lim, J, Tan, C, Agarwal, SK, Leyland, NA, and Foster, WG (2019). Melatonin activity and receptor expression in endometrial tissue and endometriosis. Human Reproduction 34, 1215–1224.
| Melatonin activity and receptor expression in endometrial tissue and endometriosis.Crossref | GoogleScholarGoogle Scholar |
Olcese, JM (2020). Melatonin and female reproduction: an expanding universe. Frontiers in Endocrinology 11, 85.
| Melatonin and female reproduction: an expanding universe.Crossref | GoogleScholarGoogle Scholar |
Ott, TL (2019). Symposium review: immunological detection of the bovine conceptus during early pregnancy. Journal of Dairy Science 102, 3766–3777.
| Symposium review: immunological detection of the bovine conceptus during early pregnancy.Crossref | GoogleScholarGoogle Scholar |
Rahman, SA, Bibbo, C, Olcese, J, Czeisler, CA, Robinson, JN, and Klerman, EB (2019). Relationship between endogenous melatonin concentrations and uterine contractions in late third trimester of human pregnancy. Journal of Pineal Research 66, e12566.
| Relationship between endogenous melatonin concentrations and uterine contractions in late third trimester of human pregnancy.Crossref | GoogleScholarGoogle Scholar |
Reiter, RJ, Tan, DX, and Galano, A (2014). Melatonin: exceeding expectations. Physiology 29, 325–333.
| Melatonin: exceeding expectations.Crossref | GoogleScholarGoogle Scholar |
Reiter, RJ, Sharma, R, Rosales-Corral, S, de Campos Zuccari, DAP, and de Almeida Chuffa, LG (2022). Melatonin: a mitochondrial resident with a diverse skill set. Life Sciences 301, 120612.
| Melatonin: a mitochondrial resident with a diverse skill set.Crossref | GoogleScholarGoogle Scholar |
Russel, AJF, Doney, JM, and Gunn, RG (1969). Subjective assessment of body fat in live sheep. The Journal of Agricultural Science 72, 451–454.
| Subjective assessment of body fat in live sheep.Crossref | GoogleScholarGoogle Scholar |
Sampaio, RV, Conceição, DSB, Miranda, MS, Sampaio, LdFS, and Ohashi, OM (2012). MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro. Reproductive Biology and Endocrinology 10, 103.
| MT3 melatonin binding site, MT1 and MT2 melatonin receptors are present in oocyte, but only MT1 is present in bovine blastocyst produced in vitro.Crossref | GoogleScholarGoogle Scholar |
Schlabritz-Loutsevitch, N, Hellner, N, Middendorf, R, Müller, D, and Olcese, J (2003). The human myometrium as a target for melatonin. The Journal of Clinical Endocrinology & Metabolism 88, 908–913.
| The human myometrium as a target for melatonin.Crossref | GoogleScholarGoogle Scholar |
Schomerus, C, Korf, H-W, Laedtke, E, Weller, JL, and Klein, DC (2000). Selective adrenergic/cyclic AMP-dependent switch-off of proteasomal proteolysis alone switches on neural signal transduction: an example from the pineal gland. Journal of Neurochemistry 75, 2123–2132.
| Selective adrenergic/cyclic AMP-dependent switch-off of proteasomal proteolysis alone switches on neural signal transduction: an example from the pineal gland.Crossref | GoogleScholarGoogle Scholar |
Sosa, C, Abecia, JA, Carriquiry, M, Vázquez, MI, Fernández-Foren, A, Talmon, M, Forcada, F, and Meikle, A (2009). Effect of undernutrition on the uterine environment during maternal recognition of pregnancy in sheep. Reproduction, Fertility and Development 21, 869–881.
| Effect of undernutrition on the uterine environment during maternal recognition of pregnancy in sheep.Crossref | GoogleScholarGoogle Scholar |
Starič, J, Farci, F, Luridiana, S, Mura, MC, Pulinas, L, Cosso, G, and Carcangiu, V (2020). Reproductive performance in three Slovenian sheep breeds with different alleles for the MTNR1A gene. Animal Reproduction Science 216, 106352.
| Reproductive performance in three Slovenian sheep breeds with different alleles for the MTNR1A gene.Crossref | GoogleScholarGoogle Scholar |
Tan, DX, Manchester, LC, Terron, MP, Flores, LJ, and Reiter, RJ (2007). One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? Journal of Pineal Research 42, 28–42.
| One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species?Crossref | GoogleScholarGoogle Scholar |
Tan, DX, Manchester, LC, Liu, X, Rosales-Corral, SA, Acuna-Castroviejo, D, and Reiter, RJ (2013). Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary functionand evolution in eukaryotes. Journal of Pineal Research 54, 127–138.
| Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary functionand evolution in eukaryotes.Crossref | GoogleScholarGoogle Scholar |
Tan, DX, Manchester, LC, Esteban-Zubero, E, Zhou, Z, and Reiter, RJ (2015). Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules 20, 18886–18906.
| Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism.Crossref | GoogleScholarGoogle Scholar |
Tao, J, Yang, M, Wu, H, Ma, T, He, C, Chai, M, Zhang, X, Zhang, J, Ding, F, Wang, S, Deng, S, Zhu, K, Song, Y, Ji, P, Liu, H, Lian, Z, and Liu, G (2018). Effects of AANAT overexpression on the inflammatory responses and autophagy activity in the cellular and transgenic animal levels. Autophagy 14, 1850–1869.
| Effects of AANAT overexpression on the inflammatory responses and autophagy activity in the cellular and transgenic animal levels.Crossref | GoogleScholarGoogle Scholar |
Tijmes, M, Pedraza, R, and Valladares, L (1996). Melatonin in the rat testis: evidence for local synthesis. Steroids 61, 65–68.
| Melatonin in the rat testis: evidence for local synthesis.Crossref | GoogleScholarGoogle Scholar |
Vázquez, MI, Forcada, F, Casao, A, Abecia, JA, Sosa, C, and Palacín, I (2010). Undernutrition and exogenous melatonin can affect the in vitro developmental competence of ovine oocytes on a seasonal basis. Reproduction in Domestic Animals 45, 677–684.
| Undernutrition and exogenous melatonin can affect the in vitro developmental competence of ovine oocytes on a seasonal basis.Crossref | GoogleScholarGoogle Scholar |
Vázquez, MI, Forcada, F, Sosa, C, Casao, A, Sartore, I, Fernández-Foren, A, Meikle, A, and Abecia, JA (2013). Effect of exogenous melatonin on embryo viability and uterine environment in undernourished ewes. Animal Reproduction Science 141, 52–61.
| Effect of exogenous melatonin on embryo viability and uterine environment in undernourished ewes.Crossref | GoogleScholarGoogle Scholar |
Vázquez I, Sosa C, Carriquiry M, Forcada F, Meikle A, Abecia J (2019) Exogenous melatonin changes oviductal gene expression in pregnant undernourished ewes during the anestrous season. In ‘Animal reproduction – proceedings of the VII International Symposium on Animal Biology of Reproduction’. p. 148. (Brazilian College of Animal Reproduction)
Xiao, L, Hu, J, Zhao, X, Song, L, Zhang, Y, Dong, W, Zhang, Q, Ma, Y, and Li, F (2018). Expression of melatonin and its related synthase and membrane receptors in the oestrous corpus luteum and corpus luteum verum of sheep. Reproduction in Domestic Animals 53, 1142–1148.
| Expression of melatonin and its related synthase and membrane receptors in the oestrous corpus luteum and corpus luteum verum of sheep.Crossref | GoogleScholarGoogle Scholar |
Xiao, L, Hu, J, Song, L, Zhang, Y, Dong, W, Jiang, Y, Zhang, Q, Yuan, L, and Zhao, X (2019). Profile of melatonin and its receptors and synthesizing enzymes in cumulus-oocyte complexes of the developing sheep antral follicle – a potential estradiol-mediated mechanism. Reproductive Biology and Endocrinology 17, 1.
| Profile of melatonin and its receptors and synthesizing enzymes in cumulus-oocyte complexes of the developing sheep antral follicle – a potential estradiol-mediated mechanism.Crossref | GoogleScholarGoogle Scholar |
Zaqout, S, Becker, LL, and Kaindl, AM (2020). Immunofluorescence staining of paraffin sections step by step. Frontiers in Neuroanatomy 14, 582218.
| Immunofluorescence staining of paraffin sections step by step.Crossref | GoogleScholarGoogle Scholar |
Zhao, H, Pang, S, and Poon, A (2002). Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment. Journal of Pineal Research 33, 140–145.
| Variations of mt1 melatonin receptor density in the rat uterus during decidualization, the estrous cycle and in response to exogenous steroid treatment.Crossref | GoogleScholarGoogle Scholar |
Zhao, D, Yu, Y, Shen, Y, Liu, Q, Zhao, Z, Sharma, R, and Reiter, RJ (2019). Melatonin synthesis and function: evolutionary history in animals and plants. Frontiers in Endocrinology 10, 249.
| Melatonin synthesis and function: evolutionary history in animals and plants.Crossref | GoogleScholarGoogle Scholar |
