Expressions of lipoprotein receptors and cholesterol efflux regulatory proteins during luteolysis in bovine corpus luteum
Kei Horihata A , Shin Yoshioka B , Masahiro Sano B , Yuki Yamamoto B , Koji Kimura B , Dariusz J. Skarzynski C and Kiyoshi Okuda A B DA Laboratory of Reproductive Physiology, Faculty of Agriculture, Okayama University, Tsushima Naka Kita-ku 1-1-1, Okayama 700-8530, Japan.
B Laboratory of Reproductive Physiology, Graduate School of Environmental and Life Science, Okayama University, Tsushima Naka Kita-ku 1-1-1, Okayama 700-8530, Japan.
C Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-747 Olsztyn, Poland.
D Corresponding author. Email: kokuda@okayama-u.ac.jp
Reproduction, Fertility and Development 29(7) 1280-1286 https://doi.org/10.1071/RD15538
Submitted: 19 December 2015 Accepted: 4 April 2016 Published: 17 May 2016
Abstract
The corpus luteum (CL) synthesises and secretes progesterone (P4), which is essential for the establishment and maintenance of pregnancy in mammals. P4 is synthesised from cholesterol. Cholesterol is internalised by low-density lipoprotein receptor (LDLR) and/or scavenger receptor B1 (SR-BI), and is effluxed by ATP-binding cassette (ABC) transporter A1 (ABCA1) and G1 (ABCG1). To test the hypothesis that lipoprotein receptors and ABC transporters are involved in functional luteolysis, we examined the expression of LDLR, SR-BI, ABCA1 and ABCG1 in bovine CL during the luteal stages and after injection of prostaglandin (PG) F2α on Day 10 after ovulation. Expression of LDLR and SR-BI mRNA and protein was lower in the regressed luteal than late luteal stage. Injection of cows with a PGF2α did not affect LDLR mRNA and protein levels in the CL. Although expression of SR-BI mRNA did not change, SR-BI protein expression decreased 12 and 24 h after PGF2α injection. The overall findings of the present study suggest that the decreased expression of SR-BI induced by PGF2α is one of the factors responsible for the continuous decrease in P4 production during functional luteolysis.
Additional keywords: luteal phase, ovary, progesterone, prostaglandin, reproduction.
References
Acosta, T. J., Bah, M. B., Korzekwa, A., Woclawek-Potocka, I., Markiewicz, W., Jaroszewski, J. J., Okuda, K., and Skarzynski, D. J. (2009). Acute changes in circulating concentrations of progesterone and nitric oxide and partial pressure of oxygen during prostaglandin F2α-induced luteolysis in cattle. J. Reprod. Dev. 55, 149–155.| Acute changes in circulating concentrations of progesterone and nitric oxide and partial pressure of oxygen during prostaglandin F2α-induced luteolysis in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtVOls7o%3D&md5=5748712674f4227780e1fa89bc841b89CAS | 19106483PubMed |
Azhar, S., Menon, M., and Menon, K. M. (1981). Receptor-mediated gonadotropin action in the ovary. Demonstration of acute dependence of rat luteal cells on exogenously supplied steroid precursor (sterols) for gonadotropin-induced steroidogenesis. Biochim. Biophys. Acta 665, 362–375.
| Receptor-mediated gonadotropin action in the ovary. Demonstration of acute dependence of rat luteal cells on exogenously supplied steroid precursor (sterols) for gonadotropin-induced steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXls1antrg%3D&md5=ee77f0ec255850fb50d0a739a82544bfCAS | 6271226PubMed |
Bogan, R. L., and Hennebold, J. D. (2010). The reverse cholesterol transport system as a potential mediator of luteolysis in the primate corpus luteum. Reproduction 139, 163–176.
| The reverse cholesterol transport system as a potential mediator of luteolysis in the primate corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWmtQ%3D%3D&md5=87b92440354d579d521a4d8e33313d13CAS | 19776099PubMed |
Connelly, M. A., and Williams, D. L. (2003). SR-BI and cholesterol uptake into steroidogenic cells. Trends Endocrinol. Metab. 14, 467–472.
| SR-BI and cholesterol uptake into steroidogenic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Whs70%3D&md5=d893d84ec8cfcc50c59e625b9c3e602aCAS | 14643062PubMed |
Ferreri, K., and Menon, K. M. (1992). Characterization and isolation of a high-density-lipoprotein-binding protein from bovine corpus luteum plasma membrane. Biochem. J. 287, 841–848.
| Characterization and isolation of a high-density-lipoprotein-binding protein from bovine corpus luteum plasma membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmsVOgtLY%3D&md5=1930b221f60a4e3313d7225aeca0ae02CAS | 1332685PubMed |
Gelissen, I. C., Harris, M., Rye, K. A., Quinn, C., Brown, A. J., Kockx, M., Cartland, S., Packianathan, M., Kritharides, L., and Jessup, W. (2006). ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler. Thromb. Vasc. Biol. 26, 534–540.
| ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFarsL0%3D&md5=e4961d3125a0d0ff0b8d4d374a099da2CAS | 16357317PubMed |
Green, R. M., Graham, M., O’Donovan, M. R., Chipman, J. K., and Hodges, N. J. (2006). Subcellular compartmentalization of glutathione: correlations with parameters of oxidative stress related to genotoxicity. Mutagenesis 21, 383–390.
| Subcellular compartmentalization of glutathione: correlations with parameters of oxidative stress related to genotoxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFyqtrbP&md5=ab41055b8f073ba2ccb5aa53b4ac0665CAS | 17012304PubMed |
Gwynne, J. T., and Strauss, J. F. (1982). The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr. Rev. 3, 299–329.
| The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlt1Smu7o%3D&md5=db52e415393e6c3e98a3720f8e6291eaCAS | 6288367PubMed |
Janowski, B. A., Willy, P. J., Devi, T. R., Falck, J. R., and Mangelsdorf, D. J. (1996). An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383, 728–731.
| An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsVGns78%3D&md5=ec6bdeff86bb1a5208288549b6beb501CAS | 8878485PubMed |
Jeon, H., and Blacklow, S. C. (2005). Structure and physiologic function of the low-density lipoprotein receptor. Annu. Rev. Biochem. 74, 535–562.
| Structure and physiologic function of the low-density lipoprotein receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsVensLo%3D&md5=37086cceb16fca4e67204075ef20c773CAS | 15952897PubMed |
Mahley, R. W., Huang, Y., and Weisgraber, K. H. (2006). Putting cholesterol in its place: apoE and reverse cholesterol transport. J. Clin. Invest. 116, 1226–1229.
| Putting cholesterol in its place: apoE and reverse cholesterol transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVWnsrw%3D&md5=fee0573c24f948f53e53c0ca80183e4fCAS | 16670767PubMed |
McCracken, J. A., Glew, M. E., and Scaramuzzi, R. J. (1970). Corpus luteum regression induced by prostaglandin F2α. J. Clin. Endocrinol. Metab. 30, 544–546.
| Corpus luteum regression induced by prostaglandin F2α.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhtFyitro%3D&md5=62b8672783d5327db4f8005616a81b9eCAS | 5435294PubMed |
McCracken, J. A., Carlson, J. C., Glew, M. E., Goding, J. R., Baird, D. T., Green, K., and Samuelsson, B. (1972). Prostaglandin F2α identified as the luteolytic hormone in sheep. Nat. New Biol. 238, 129–134.
| Prostaglandin F2α identified as the luteolytic hormone in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XkvF2iurk%3D&md5=82f93bcef25d8d71ca8eca8235bfc809CAS | 4506189PubMed |
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=8cdd014958790bd79e4fe05b2d98abb0CAS | 10221982PubMed |
Miranda-Jiménez, L., and Murphy, B. D. (2007). Lipoprotein receptor expression during luteinization of the ovarian follicle. Am. J. Physiol. Endocrinol. Metab. 293, E1053–E1061.
| Lipoprotein receptor expression during luteinization of the ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 17698983PubMed |
Miyamoto, Y., Skarzynski, D. J., and Okuda, K. (2000). Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle? Biol. Reprod. 62, 1109–1115.
| Is tumor necrosis factor α a trigger for the initiation of endometrial prostaglandin F2α release at luteolysis in cattle?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisl2htr8%3D&md5=408fd4fd49a7fe8e42996658b2b0658cCAS | 10775155PubMed |
Motta, A. B., Estevez, A., Franchi, A., Perez-Martinez, S., Farina, M., Ribeiro, M. L., Lasserre, A., and Gimeno, M. F. (2001). Regulation of lipid peroxidation by nitric oxide and PGF2α during luteal regression in rats. Reproduction 121, 631–637.
| Regulation of lipid peroxidation by nitric oxide and PGF2α during luteal regression in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFKgsbw%3D&md5=2d623c76b3bf02d472f53bce8b96c0d4CAS | 11277883PubMed |
Ohtani, M., Kobayashi, S., Miyamoto, A., Hayashi, K., and Fukui, Y. (1998). Real-time relationships between intraluteal and plasma concentrations of endothelin, oxytocin, and progesterone during prostaglandin F2α-induced luteolysis in the cow. Biol. Reprod. 58, 103–108.
| Real-time relationships between intraluteal and plasma concentrations of endothelin, oxytocin, and progesterone during prostaglandin F2α-induced luteolysis in the cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhvVSjsg%3D%3D&md5=15b0045f58ee2aa537d20c81ac96e390CAS | 9472929PubMed |
Sakumoto, R., Vermehren, M., Kenngott, R. A., Okuda, K., and Sinowatz, F. (2011). Localization of gene and protein expressions of tumor necrosis factor-α and tumor necrosis factor receptor types I and II in the bovine corpus luteum during the estrous cycle. J. Anim. Sci. 89, 3040–3047.
| Localization of gene and protein expressions of tumor necrosis factor-α and tumor necrosis factor receptor types I and II in the bovine corpus luteum during the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MfkvFKmtg%3D%3D&md5=358827b67d8a0ada2bd816de3eeee8bbCAS | 21551345PubMed |
Silvia, W. J., Lewis, G. S., McCracken, J. A., Thatcher, W. W., and Wilson, L. (1991). Hormonal regulation of uterine secretion of prostaglandin F2α during luteolysis in ruminants. Biol. Reprod. 45, 655–663.
| Hormonal regulation of uterine secretion of prostaglandin F2α during luteolysis in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslSktbw%3D&md5=69a9778a764d9f4162a7b70e73270c7bCAS | 1756203PubMed |
Sticozzi, C., Belmonte, G., Pecorelli, A., Cervellati, F., Leoncini, S., Signorini, C., Ciccoli, L., De Felice, C., Hayek, J., and Valacchi, G. (2013). Scavenger receptor B1 post-translational modifications in Rett syndrome. FEBS Lett. 587, 2199–2204.
| Scavenger receptor B1 post-translational modifications in Rett syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovVChsbY%3D&md5=85c3b764c5bab65de3fa9ec4d1e9376fCAS | 23711372PubMed |
Sugino, N., and Okuda, K. (2007). Species-related differences in the mechanism of apoptosis during structural luteolysis. J. Reprod. Dev. 53, 977–986.
| Species-related differences in the mechanism of apoptosis during structural luteolysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOls7nJ&md5=e479e3613022531db8089cdb7182346cCAS | 17984567PubMed |
Tontonoz, P., and Mangelsdorf, D. J. (2003). Liver X receptor signaling pathways in cardiovascular disease. Mol. Endocrinol. 17, 985–993.
| Liver X receptor signaling pathways in cardiovascular disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlymsb8%3D&md5=739ca3b0a267f26badb947096e4cc01eCAS | 12690094PubMed |
Vandenabeele, P., Declercq, W., Beyaert, R., and Fiers, W. (1995). Two tumour necrosis factor receptors: structure and function. Trends Cell Biol. 5, 392–399.
| Two tumour necrosis factor receptors: structure and function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovValsrY%3D&md5=7f7cc2c656f9b3e86c0b9382e1f0ee91CAS | 14732063PubMed |
Wang, N., Lan, D., Chen, W., Matsuura, F., and Tall, A. R. (2004). ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl Acad. Sci. USA 101, 9774–9779.
| ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVaht7g%3D&md5=31be9d6e6219fea32aa602a5dce1b5cbCAS | 15210959PubMed |
Zhuang, J., Zhang, H., Zhou, R., Chen, L., Chen, J., and Shen, X. (2013). Regulation of prostaglandin F2α against β amyloid clearance and its inflammation induction through LXR/RXR heterodimer antagonism in microglia. Prostaglandins Other Lipid Mediat. 106, 45–52.
| Regulation of prostaglandin F2α against β amyloid clearance and its inflammation induction through LXR/RXR heterodimer antagonism in microglia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvV2qtr%2FO&md5=761ec1ce0a3ca7922b39a7b235935760CAS | 24076168PubMed |