Expression of Progesterone Receptor Membrane Component 1 (PGRMC1) in Follicular and Luteal Tissues in Goats – Effect of Short-term Concentrate Supplementation
Abstract
This study evaluated the effects of short-term supplementation with concentrate on ovulation rate, plasma progesterone concentrations and gene expression for Progesterone Receptor Membrane Component 1 (PGRMC1) in ovarian tissues of Boer goats. Twenty females were allocated to two groups: 1) Control, receiving a maintenance diet consisting of 70% Napier grass plus 30% concentrate (4.45 MJ/day); 2) Supplemented, receiving twice their required metabolizable energy for maintenance by adding extra concentrate (8.90 MJ/day). The dietary treatments were applied for 25 days, beginning 5 days before (Day 5) CIDR removal (Day 0). On Day 19, the ovulation rate was estimated by trans-rectal ultrasonographic scanning. Blood was sampled for progesterone (P4) analysis every 2 days, from Days 9 to 27. On Day 27, the level of expression of PGRMC1 was assessed in follicles and corpora lutea. The ovulation rate was not affected by treatment (Control 1.00 ± 0.24; Supplemented 1.25 ± 0.25). Over Days 13 to 27, plasma P4 concentrations were significantly (p<0.05) greater in the Supplemented group than in the Control group. The expression of PGRMC1 in follicular and luteal tissues was greater in the Supplemented group than in the Control group (p<0.05). There was a positive correlation between PGRMC1 expression and P4 concentration (r= 0.65, p<0.05). It was concluded that, in goats, short-term concentrate supplementation could increase P4 concentrations, at least in part, by influencing the expression of PGRMC1. This finding suggests that short-term concentrate supplementation can support embryo development during the luteal phase and early stages of pregnancy.
References
Abolghasemi, A., Dirandeh, E., Ansari Pirsaraei, Z., & Shohreh, B. Dietary conjugated linoleic acid supplementation alters the expression of genes involved in the endocannabinoid system in the bovine endometrium and increases plasma progesterone concentrations. Theriogenology, 86(6), 1453-1459. https://doi.org/10.1016/j.theriogenology.2016.05.003
Banchero, G. E., Stefanova, K., Lindsay, D. R., Quintans, G., Baldi, F., Milton, J. T. B., & Martin, G. B. (2021). Ovulation and ovulation rate in ewes under grazing conditions: factors affecting the response to short-term supplementation. Animal, 15, 100100. https://doi.org/10.1016/j.animal.2020.100100
Bomfim, G. F., Merighe, G. K. F., de Oliveira, S. A., Rodrigues, A. D., Augusto, L., Teixeira, I. A. M. A., de Resende, K. T., & Negrao, J. A. (2016). Effects of different supplemental soya bean oil levels on the performance of prepubertal Saanen goats: Oestrogen and progesterone release. Journal of Animal Physiology and Animal Nutrition, 100(6), 1097–1103. https://doi.org/10.1111/jpn.12486
Celestino, J. J. H., Bruno, J. B., Lima-Verde, I. B., Matos, M. H. T., Saraiva, M. V. A., Chaves, R. N., Martins, F. S., Almeida, A. P., Cunha, R. M. S., Lima, L. F., Khesller, P. O., Campello, C. C., Silva, J. R. V., Báo, S. N., & Figueiredo, J. R. (2010). Steady-state level of kit ligand mRNA in goat ovaries and the role of kit ligand in preantral follicle survival and growth in vitro. Molecular Reproduction and Development, 77(3), 231–240. https://doi.org/10.1002/mrd.21138
Chaudhari, R. K., Mahla, A. S., Singh, S. K., Pawde, A. M., Badasara, S. K., Kumar, H., Patra, M. K., & Krishnaswamy, N. (2020). Effect of dietary n-3 polyunsaturated fatty acid supplementation on the expression of genes involved in progesterone biosynthesis in the corpus luteum of goat (Capra hircus). Reproduction in Domestic Animals, 55(6), 1166–1177. https://doi.org/10.1111/rda.13757
Frota, I. M. A., Leitão, C. C. F., Costa, J. J. N., Brito, I. R., van Den Hurk, R., & Silva, J. R. V. (2011). Stability of housekeeping genes and expression of locally produced growth factors and hormone receptors in goat preantral follicles. Zygote, 19(1), 71–83. https://doi.org/10.1017/S0967199410000080
Grazul-Bilska, A. T., Thammasiri, J., Kraisoon, A., Reyaz, A., Bass, C. S., Kaminski, S. L., Navanukraw, C., & Redmer, D. A. (2018). Expression of progesterone receptor protein in the ovine uterus during the estrous cycle: effects of nutrition, arginine and FSH. Theriogenology, 108, 7–15. https://doi.org/10.1016/j.theriogenology.2017.11.008
Haruna, S., Kuroiwa, T., Lu, W., Zabuli, J., Tanaka, T., & Kamomae, H. (2009). The effects of short-term nutritional stimulus before and after the luteolysis on metabolic status, reproductive hormones and ovarian activity in goats. Journal of Reproduction and Development, 55(1), 39–44. https://doi.org/10.1262/jrd.20082
Juengel, J. L., Cushman, R. A., Dupont, J., Fabre, S., Lea, R. G., Martin, G. B., Mossa, F., Pitman, J. L., Price, C. A., & Smith, P. (2021). The ovarian follicle of ruminants: The path from conceptus to adult. Reproduction, Fertility and Development, 33(10), 621–642. https://doi.org/10.1071/RD21086
Kandiel, M. M. M., Watanabe, G., Sosa, G. A., Abou El-Roos, M. E. A., Abdel-Ghaffar, A. E., Li, J. Y., Manabe, N., El Azab, A. E. S. I., & Taya, K. (2010). Profiles of circulating steroid hormones, gonadotropins, immunoreactive inhibin and prolactin during pregnancy in goats and immunolocalization of inhibin subunits, steroidogenic enzymes and prolactin in the corpus luteum and placenta. Journal of Reproduction and Development, 56(2), 243–250. https://doi.org/10.1262/jrd.09-159S
Kowalik, M. K., & Kotwica, J. (2008). Progesterone receptor membrane component 1 (PGRMC1) gene expression in corpus luteum during the estrous cycle in cows. Reproductive Biology, 8(3), 291–297. https://doi.org/10.1016/s1642-431x(12)60019-9
Kowalik, M. K., Rekawiecki, R., & Kotwica, J. (2014). Expression and localization of progesterone receptor membrane component 1 and 2 and serpine mRNA binding protein 1 in the bovine corpus luteum during the estrous cycle and the first trimester of pregnancy. Theriogenology, 82(8), 1086–1093. https://doi.org/10.1016/j.theriogenology.2014.07.021
Lepesheva, G. I., & Waterman, M. R. (2007). Sterol 14α-demethylase cytochrome P450 (CYP51), a P450 in all biological kingdoms. Biochimica et Biophysica Acta, 1770(3), 467–477. https://doi.org/10.1016/j.bbagen.2006.07.018
Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 25(4), 402–408. https://doi.org/10.1006/meth.2001.1262
Manna, P. R., Stetson, C. L., Slominski, A. T., & Pruitt, K. (2016). Role of the steroidogenic acute regulatory protein in health and disease. Endocrine, 51(1), 7–21. https://doi.org/10.1007/s12020-015-0715-6
Martinez, I. Y. H, Santos, A. P. C, Bottino, M. P., Orlandi, R. E., Santos, G., Simões, L. M. S., Souza, J. C., Diaza, A. M. G., Binelli, M., & Sales, J. N. S. (2018). Molecular and endocrine factors involved in future dominant follicle dynamics during the induction of luteolysis in Bos indicus cows. Theriogenology, 111, 78–83. https://doi.org/10.1016/j.theriogenology.2018.01.019
McKay, Z. C., Lynch, M. B., Mulligan, F. J., Rajauria, G., Miller, C., & Pierce, K. M. (2019). The effect of concentrate supplementation type on milk production, dry matter intake, rumen fermentation, and nitrogen excretion in late-lactation, spring-calving grazing dairy cows. Journal of Dairy Science, 102(6), 5042–5053. https://doi.org/10.3168/jds.2018-15796
Meza-Herrera, C. A., Santamaría-Estrada, C. E., Flores-Hernández, A., Cano-Villegas, O., de la Peña, C. G., Macias-Cruz, U., Calderón-Leyva, G., Ángel-García, O., Mellado, M., Carrillo-Moreno, D., & Véliz-Deras, F. G. (2019). The Opuntia effect upon the out-of-season embryo implantation rate in goats: corpus luteal number, corpus luteal diameter and serum progesterone concentrations. Livestock Science, 228, 201–206. https://doi.org/10.1016/J.LIVSCI.2019.09.002
Meza-Herrera, C. A., Vargas-Beltran, F., Tena-Sempere, M., González-Bulnes, A., Macias-Cruz, U., & Veliz-Deras, F. G. (2013). Short-term beta-carotene-supplementation positively affects ovarian activity and seruminsulin concentrations in a goatmodel. Journal of Endocrinological Investigation, 36(3), 185–189. https://doi.org/10.3275/8410
Nogueira, D. M., Cavalieri, J., Fitzpatrick, L. A., Gummow, B., Blache, D., & Parker, A. J. (2016). Effect of hormonal synchronisation and/or short-term supplementation with maize on follicular dynamics and hormone profiles in goats during the non-breeding season. Animal Reproduction Science, 171, 87–97. https://doi.org/10.1016/j.anireprosci.2016.06.003
Nogueira, D. M., Eshtaeba, A., Cavalieri, J., Fitzpatrick, L. A., Gummow, B., Blache, D., & Parker, A. J. (2017). Short-term supplementation with maize increases ovulation rate in goats when dietary metabolizable energy provides requirements for both maintenance and 1.5 times maintenance. Theriogenology, 89, 97–105. https://doi.org/10.1016/j.theriogenology.2016.10.014
Norhazirah, A. H., Shohaimi, R., & Maidin, M. S. (2016). Assessment of reproductive performance and abortion occurrence of Boer goats as influenced by farm systems and feeding practices. Malaysian Society of Animal Production, 19(2), 107-115.
Parr, R. A., Davis, I. F., Miles, M. A. & Squires, T. J. (1993). Feed intake affects metabolic clearance rate of progesterone in sheep. Research in Veterinary Science, 55(3), 306–310. https://doi.org/10.1016/0034-5288(93)90099-2
Peluso, J. J., Pru, C. A., Liu, X., Kelp, N. C., & Pru, J. K. (2019). Progesterone receptor membrane component 1 and 2 regulate granulosa cell mitosis and survival through an NFκB-dependent mechanism. Biology of Reproduction, 100(6), 1571–1580. https://doi.org/10.1093/biolre/ioz043
Peluso, J. J., & Pru, J. K. (2014). Non-canonical progesterone signaling in granulosa cell function. Reproduction, 147(5), 169–178. https://doi.org/10.1530/REP-13-0582
Putranto, H. D., Hasibuan, G. P., Yumiati, Y., & Ginting, S. M. (2017). Effect of katuk (Sauropus androgynus) powder supplementation on the levels of progesterone (P4) and estradiol-17β (E2) hormones in kacang goat (Capra aegagrus). Nusantara Bioscience, 9(1), 86–91. https://doi.org/10.13057/nusbiosci/n090115
Rekawiecki, R., Kowalik, M. K., & Kotwica, J. (2017). Steroid hormone receptors in the corpus luteum. In: R. Meidan (Ed.), The Life Cycle of the Corpus Luteum (pp. 79-97). Springer. https://doi.org/10.1007/978-3-319-43238-0_5
Robertson, S. M., Clayton, E. H., Morgan, B., & Friend, M. A. (2015). Reproductive performance in ewes fed varying levels of cut lucerne pasture around conception. Animal Reproduction Science, 158, 75–85. https://doi.org/10.1016/j.anireprosci.2015.05.001
ShikhMaidin, M., Blackberry, M. A., Milton, J. T. B., Hawken, P. A. R., & Martin, G. B. (2014). Nutritional supplements, leptin, insulin and progesterone in female Australian cashmere goats. APCBEE Procedia, 8, 299–304. https://doi.org/10.1016/j.apcbee.2014.03.044
Stocco, D., & Selvaraj, V. (2017). Yet another scenario in the regulation of the steroidogenic acute regulatory (STAR) protein gene. Endocrinology, 158(2), 235–238. https://doi.org/10.1210/en.2016-1874
Sueldo, C., Liu, X., & Peluso, J. J. (2015). Progestin and AdipoQ Receptor 7, Progesterone Membrane Receptor Component 1 (PGRMC1), and PGRMC2 and their role in regulating progesterone’s ability to suppress human granulosa/luteal cells from entering into the cell cycle. Biology of Reproduction, 93(3), 1–11. https://doi.org/10.1095/biolreprod.115.131508
Terzaghi, L., Luciano, A., & Lodde, V. (2015). Progesterone receptor membrane component-1 in cell division: its role in bovine granulosa cells mitosis. International Journal of Health, Animal Science and Food Safety, 2(1s). https://doi.org/10.13130/2283-3927/5114
Widiani, I. A. K., Bidura, I. G.N.G., & Putri, B. R. T. (2020). Performance of fattening Bali cattle on feedlot systems which are provided by local grass and concentrate supplementation. International Journal of Fauna and Biological Studies, 7, 07–10.
Worku, A., Urge, M., Animut, G., & Asefa, G. (2020). Comparative slaughter performance and meat quality of Rutana, Gumuz and Washera sheep of Ethiopia supplemented with different levels of concentrate. Open Journal of Animal Sciences, 10, 48–63. https://doi.org/10.4236/ojas.2020.101005
Yang, T., Espenshade, P. J., Wright, M. E., Yabe, D., Gong, Y., Aebersold, R., Goldstein, J. L., & Brown, M. S. (2002). Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER. Cell, 110(4), 489–500. https://doi.org/10.1016/S0092-8674(02)00872-3
Yuan, X.-H., Yang, C.-R., Wang, X.-N., Zhang, L.-L., Gao, X.-R., & Shi, Z.-Y. (2018). Progesterone maintains the status of granulosa cells and slows follicle development partly through PGRMC1. Journal of Cellular Physiology, 234, 709–720. https://doi.org/10.1002/jcp.26869
Zabuli, J., Tanaka, T., Lu, W., & Kamomae, H. (2010). Intermittent nutritional stimulus by short-term treatment of high-energy diet promotes ovarian performance together with increases in blood levels of glucose and insulin in cycling goats. Animal Reproduction Science, 122(3-4), 288≠293. https://doi.org/10.1016/j.anireprosci.2010.09.005
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