Roles of vitamin D and its receptor in the proliferation and apoptosis of luteinised granulosa cells in the goat
Xiaolei Yao A , Zhibo Wang A , M. A. El-Samahy A , Caifang Ren A , Zifei Liu A , Feng Wang
A B D and Peihua You C
+ Author Affiliations
- Author Affiliations
A Jiangsu Livestock Embryo Engineering Laboratory, Nanjing Agricultural University, Nanjing 210095, P. R. China.
B National Experimental Teaching Demonstration Centre of Animal Science, Nanjing Agricultural University, Nanjing 210095, P. R. China.
C Portal Agri-Industries Co., Ltd, Xingdian Street, Pikou District, Nanjing 210095, P. R. China.
D Corresponding author. Email: caeet@njau.edu.cn
Reproduction, Fertility and Development 32(3) 335-348 https://doi.org/10.1071/RD18442
Submitted: 7 November 2018 Accepted: 16 June 2019 Published: 11 November 2019
Abstract
The objective of this study was to investigate the dose-dependent effect of 1α,25-(OH)2VD3 (Vit D3) on in vitro proliferation of goat luteinised granulosa cells (LGCs) and to determine the underlying mechanisms of its action by overexpressing and silencing vitamin D receptor (VDR) in LGCs. Results showed that VDR was prominently localised in GCs and theca cells (TCs) and its expression increased with follicle diameter, but was lower in atretic follicles than in healthy follicles. The proliferation rate of LGCs was significantly higher in the Vit D3-treated groups than in the control group, with the highest proliferation rate observed in the 10 nM group; this was accompanied by changes in the expression of cell cycle-related genes. These data indicate that Vit D3 affects LGC proliferation in a dose-dependent manner. Contrary to the VDR knockdown effects, its overexpression upregulated and downregulated cell cycle- and apoptosis-related genes respectively; moreover, supplementation with 10 nM of Vit D3 significantly enhanced these effects. These results suggest that changes in VDR expression patterns in LGCs may be associated with follicular development by regulation of cell proliferation and apoptosis. These findings will enhance the understanding of the roles of Vit D3 and VDR in goat ovarian follicular development.
Additional keywords: 1α,25-(OH)2VD3, follicular development, ovary.
References
Alabsi, A. M., Lim, K. L., Paterson, I. C., Ali-Saeed, R., and Muharram, B. A. (2016). Cell cycle arrest and apoptosis induction via modulation of mitochondrial integrity by Bcl-2 family members and caspase dependence in Dracaena cinnabari-treated H400 human oral squamous cell carcinoma. BioMed Res. Int. 2016, 4904016.| Cell cycle arrest and apoptosis induction via modulation of mitochondrial integrity by Bcl-2 family members and caspase dependence in Dracaena cinnabari-treated H400 human oral squamous cell carcinoma.Crossref | GoogleScholarGoogle Scholar | 27123447PubMed |
Alimirah, F., Vaishnav, A., McCormick, M., Echchgadda, I., Chatterjee, B., Mehta, R. G., and Peng, X. J. (2010). Functionality of unliganded VDR in breast cancer cells: repressive action on CYP24 basal transcription. Mol. Cell. Biochem. 342, 143–150.
| Functionality of unliganded VDR in breast cancer cells: repressive action on CYP24 basal transcription.Crossref | GoogleScholarGoogle Scholar | 20440542PubMed |
Asselin, E., Xiao, C. W., Wang, Y. F., and Tsang, B. K. (2000). Mammalian follicular development and atresia: role of apoptosis. Biol. Signals Recept. 9, 87–95.
| Mammalian follicular development and atresia: role of apoptosis.Crossref | GoogleScholarGoogle Scholar | 10810203PubMed |
Boisen, I. M., Bollehuus Hansen, L., Mortensen, L. J., Lanske, B., Juul, A., and Blomberg Jensen, M. (2017). Possible influence of vitamin D on male reproduction. J. Steroid Biochem. Mol. Biol. 173, 215–222.
| Possible influence of vitamin D on male reproduction.Crossref | GoogleScholarGoogle Scholar | 27693423PubMed |
Carlberg, C., and Campbell, M. J. (2013). Vitamin D receptor signaling mechanisms: integrated actions of a well-defined transcription factor. Steroids 78, 127–136.
| Vitamin D receptor signaling mechanisms: integrated actions of a well-defined transcription factor.Crossref | GoogleScholarGoogle Scholar | 23178257PubMed |
Chen, Y., Sun, Z., Xu, J., Wang, P., Tang, J., Shi, X., Liu, J., Ren, F., and Xu, L. (2018a). Vitamin D and DDX4 regulate the proliferation and invasion of ovarian cancer cells. Oncol. Lett. 16, 905–909.
| 29963162PubMed |
Chen, Y., Liu, X., Zhang, F., Liao, S., He, X., Zhuo, D., Huang, H., and Wu, Y. (2018b). Vitamin D receptor suppresses proliferation and metastasis in renal cell carcinoma cell lines via regulating the expression of the epithelial Ca2+ channel TRPV5. Plos One 13, e0195844.
| Vitamin D receptor suppresses proliferation and metastasis in renal cell carcinoma cell lines via regulating the expression of the epithelial Ca2+ channel TRPV5.Crossref | GoogleScholarGoogle Scholar | 30596758PubMed |
Chiang, K. C., Yeh, C. N., Pang, J. H. S., Hsu, J. T., Yeh, T. S., Chen, L. W., Kuo, S. F., Hsieh, P. J., Pan, Y. C., Takano, M., Chen, T. C., Feng, T. H., Kittaka, A., and Juang, H. H. (2016). 1 alpha,25(OH)(2)D-3 Analog, MART-10, inhibits neuroendocrine tumor cell growth through induction of G(0)/G(1) cell-cycle arrest and apoptosis. Anticancer Res. 36, 3307–3313.
| 27354587PubMed |
Chiang, K. C., Yeh, T. S., Huang, C. C., Chang, Y. C., Juang, H. H., Cheng, C. T., Pang, J. H. S., Hsu, J. T., Takano, M., Chen, T. C., Kittaka, A., Hsiao, M., and Yeh, C. N. (2017). MART-10 represses cholangiocarcinoma cell growth and high vitamin D receptor expression indicates better prognosis for cholangiocarcinoma. Sci. Rep. 7, 43773-43784.
| MART-10 represses cholangiocarcinoma cell growth and high vitamin D receptor expression indicates better prognosis for cholangiocarcinoma.Crossref | GoogleScholarGoogle Scholar | 28256614PubMed |
Cong, M., Wen, L. L., Han, F., Xu, Y. H., and Shi, Y. X. (2017). Alterations in cyclin D1 and cyclin-dependent kinase 4 expression in the amygdalae of post-traumatic stress disorder rats. Mol. Med. Rep. 16, 8351–8358.
| Alterations in cyclin D1 and cyclin-dependent kinase 4 expression in the amygdalae of post-traumatic stress disorder rats.Crossref | GoogleScholarGoogle Scholar | 28983608PubMed |
Consiglio, M., Destefanis, M., Morena, D., Foglizzo, V., Forneris, M., Pescarmona, G., and Silvagno, F. (2014). The vitamin D receptor inhibits the respiratory chain, contributing to the metabolic switch that is essential for cancer cell proliferation. Plos One 9, e115816.
| The vitamin D receptor inhibits the respiratory chain, contributing to the metabolic switch that is essential for cancer cell proliferation.Crossref | GoogleScholarGoogle Scholar | 25546457PubMed |
Dowd, D. R., and MacDonald, P. N. (2010). The 1,25-dihydroxyvitamin D3-independent actions of the vitamin D receptor in skin. J. Steroid Biochem. Mol. Biol. 121, 317–321.
| The 1,25-dihydroxyvitamin D3-independent actions of the vitamin D receptor in skin.Crossref | GoogleScholarGoogle Scholar | 20362670PubMed |
Emam, M. A., Abouelroos, M. E. A., and Gad, F. A. (2016). Expression of calbindin-D9k and vitamin D receptor in the uterus of Egyptian buffalo during follicular and luteal phases. Acta Histochem. 118, 471–477.
| Expression of calbindin-D9k and vitamin D receptor in the uterus of Egyptian buffalo during follicular and luteal phases.Crossref | GoogleScholarGoogle Scholar | 27142230PubMed |
Emanuelsson, I., Wikvall, K., Friman, T., and Norlin, M. (2018). Vitamin D analogues tacalcitol and calcipotriol inhibit proliferation and migration of T98G human glioblastoma cells. Basic Clin. Pharmacol. Toxicol. 123, 130–136.
| Vitamin D analogues tacalcitol and calcipotriol inhibit proliferation and migration of T98G human glioblastoma cells.Crossref | GoogleScholarGoogle Scholar | 29575677PubMed |
Fang, Z., Zhang, L., Liao, Q., Wang, Y., Yu, F., Feng, M., Xiang, X., and Xiong, J. (2017). Regulation of TRIM24 by miR-511 modulates cell proliferation in gastric cancer. J. Exp. Clin. Cancer Res. 36, 17-27.
| Regulation of TRIM24 by miR-511 modulates cell proliferation in gastric cancer.Crossref | GoogleScholarGoogle Scholar |
Grundmann, M., Haidar, M., Placzko, S., Niendorf, R., Darashchonak, N., Hubel, C. A., and von Versen-Hoynck, F. (2012). Vitamin D improves the angiogenic properties of endothelial progenitor cells. Am. J. Physiol. Cell Physiol. 303, C954–C962.
| Vitamin D improves the angiogenic properties of endothelial progenitor cells.Crossref | GoogleScholarGoogle Scholar | 22932684PubMed |
Grzesiak, M., Waszkiewicz, E., Wojtas, M., Kowalik, K., and Franczak, A. (2019). Expression of vitamin D receptor in the porcine uterus and effect of 1,25(OH)2D3 on progesterone and estradiol-17beta secretion by uterine tissues in vitro. Theriogenology 125, 102–108.
| Expression of vitamin D receptor in the porcine uterus and effect of 1,25(OH)2D3 on progesterone and estradiol-17beta secretion by uterine tissues in vitro.Crossref | GoogleScholarGoogle Scholar | 30399506PubMed |
Hatzirodos, N., Irving-Rodgers, H. F., Hummitzsch, K., Harland, M. L., Morris, S. E., and Rodgers, R. J. (2014). Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics 15, 24-42.
| Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes.Crossref | GoogleScholarGoogle Scholar |
He, L., Liu, T. J., Shi, Y. Y., Tian, F., Hu, H. Y., Deb, D. K., Chen, Y. Y., Bissonnette, M., and Li, Y. C. (2018). Gut epithelial vitamin D receptor regulates microbiota-dependent mucosal inflammation by suppressing intestinal epithelial cell apoptosis. Endocrinology 159, 967–979.
| Gut epithelial vitamin D receptor regulates microbiota-dependent mucosal inflammation by suppressing intestinal epithelial cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 29228157PubMed |
Herian, M., Luck, M. R., and Grzesiak, M. (2018). The influence of testosterone on the expression and function of vitamin D(3) receptor (VDR) protein in the porcine ovarian follicle. Physiol. Res. 67, 515–519.
| The influence of testosterone on the expression and function of vitamin D(3) receptor (VDR) protein in the porcine ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 29527916PubMed |
Hong, S. H., Lee, J. E., An, S. M., Shin, Y. Y., Hwang, D. Y., Yang, S. Y., Cho, S. K., and An, B. S. (2017). Effect of vitamin D3 on biosynthesis of estrogen in porcine granulosa cells via modulation of steroidogenic enzymes. Toxicol. Res. 33, 49–54.
| Effect of vitamin D3 on biosynthesis of estrogen in porcine granulosa cells via modulation of steroidogenic enzymes.Crossref | GoogleScholarGoogle Scholar | 28133513PubMed |
Huet, T., Laverny, G., Ciesielski, F., Molnar, F., Ramamoorthy, T. G., Belorusova, A. Y., Antony, P., Potier, N., Metzger, D., Moras, D., and Rochel, N. (2015). A vitamin D receptor selectively activated by gemini analogs reveals ligand dependent and independent effects. Cell Reports 10, 516–526.
| A vitamin D receptor selectively activated by gemini analogs reveals ligand dependent and independent effects.Crossref | GoogleScholarGoogle Scholar | 25620699PubMed |
Irani, M., and Merhi, Z. (2014). Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review. Fertil. Steril. 102, 460–468.e3.
| Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review.Crossref | GoogleScholarGoogle Scholar | 24933120PubMed |
Kaipia, A., and Hsueh, A. J. W. (1997). Regulation of ovarian follicle atresia. Annu. Rev. Physiol. 59, 349–363.
| Regulation of ovarian follicle atresia.Crossref | GoogleScholarGoogle Scholar | 9074768PubMed |
Kinuta, K., Tanaka, H., Moriwake, T., Aya, K., Kato, S., and Seino, Y. (2000). Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 141, 1317–1324.
| Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads.Crossref | GoogleScholarGoogle Scholar | 10746634PubMed |
Knabl, J., Vattai, A., Ye, Y., Jueckstock, J., Hutter, S., Kainer, F., Mahner, S., and Jeschke, U. (2017). Role of placental VDR expression and function in common late pregnancy disorders. Int. J. Mol. Sci. 18, 2340-2357.
| Role of placental VDR expression and function in common late pregnancy disorders.Crossref | GoogleScholarGoogle Scholar | 29113124PubMed |
Koike, T., Fukuda, N., Fukagawa, M., Ohta, K., and Kurokawa, K. (1997). Correlation of enhanced cell proliferation with decreased density of vitamin D receptor in parathyroid hyperplasia in chronic dialysis patients. Nephrology (Carlton) 3, 279–284.
| Correlation of enhanced cell proliferation with decreased density of vitamin D receptor in parathyroid hyperplasia in chronic dialysis patients.Crossref | GoogleScholarGoogle Scholar |
Kovalenko, P. L., Clinton, S. K., and Fleet, J. C. (2011). Deletion of vitamin D receptor in prostate epithelial cells increases proliferation, reduces apoptosis, and enhances early carcinogenesis in the TgAPT121 mouse model of prostate cancer. Cancer Res. 71, Abstract nr 813.
| Deletion of vitamin D receptor in prostate epithelial cells increases proliferation, reduces apoptosis, and enhances early carcinogenesis in the TgAPT121 mouse model of prostate cancer.Crossref | GoogleScholarGoogle Scholar |
Lee, S. M., and Pike, J. W. (2016). The vitamin D receptor functions as a transcription regulator in the absence of 1,25-dihydroxyvitamin D3. J. Steroid Biochem. Mol. Biol. 164, 265–270.
| The vitamin D receptor functions as a transcription regulator in the absence of 1,25-dihydroxyvitamin D3.Crossref | GoogleScholarGoogle Scholar | 26323657PubMed |
Lee, C. T., Wang, J. Y., Chou, K. Y., and Hsu, M. I. (2014). 1,25-Dihydroxyvitamin D3 increases testosterone-induced 17beta-estradiol secretion and reverses testosterone-reduced connexin 43 in rat granulosa cells. Reprod. Biol. Endocrinol. 12, 90-101.
| 1,25-Dihydroxyvitamin D3 increases testosterone-induced 17beta-estradiol secretion and reverses testosterone-reduced connexin 43 in rat granulosa cells.Crossref | GoogleScholarGoogle Scholar | 25239217PubMed |
Lorenzen, M., Boisen, I. M., Mortensen, L. J., Lanske, B., Juul, A., and Blomberg Jensen, M. (2017). Reproductive endocrinology of vitamin D. Mol. Cell. Endocrinol. 453, 103–112.
| Reproductive endocrinology of vitamin D.Crossref | GoogleScholarGoogle Scholar | 28342856PubMed |
Matsuda, F., Inoue, N., Manabe, N., and Ohkura, S. (2012). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev. 58, 44–50.
| Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells.Crossref | GoogleScholarGoogle Scholar | 22450284PubMed |
Merhi, Z., Doswell, A., Krebs, K., and Cipolla, M. (2014). Vitamin D alters genes involved in follicular development and steroidogenesis in human cumulus granulosa cells. J. Clin. Endocrinol. Metab. 99, E1137–E1145.
| Vitamin D alters genes involved in follicular development and steroidogenesis in human cumulus granulosa cells.Crossref | GoogleScholarGoogle Scholar | 24628555PubMed |
Merhi, Z., Buyuk, E., and Cipolla, M. J. (2018). Advanced glycation end products alter steroidogenic gene expression by granulosa cells: an effect partially reversible by vitamin D. Mol. Hum. Reprod. 24, 318–326.
| Advanced glycation end products alter steroidogenic gene expression by granulosa cells: an effect partially reversible by vitamin D.Crossref | GoogleScholarGoogle Scholar | 29538679PubMed |
Moor, R. M., Hay, M. F., Dott, H. M., and Cran, D. G. (1978). Macroscopic identification and steroidogenic function of atretic follicles in sheep. J. Endocrinol. 77, 309–318.
| Macroscopic identification and steroidogenic function of atretic follicles in sheep.Crossref | GoogleScholarGoogle Scholar | 660074PubMed |
Nguyen, T. P. H., Yong, H. E. J., Chollangi, T., Borg, A. J., Brennecke, S. P., and Murthi, P. (2015). Placental vitamin D receptor expression is decreased in human idiopathic fetal growth restriction. J. Mol. Med. (Berl) 93, 795–805.
| Placental vitamin D receptor expression is decreased in human idiopathic fetal growth restriction.Crossref | GoogleScholarGoogle Scholar |
Nguyen, T. P. H., Yong, H. E. J., Chollangi, T., Brennecke, S. P., Fisher, S. J., Wallace, E. M., Ebeling, P. R., and Murthi, P. (2018). Altered downstream target gene expression of the placental Vitamin D receptor in human idiopathic fetal growth restriction. Cell Cycle 17, 182–190.
| Altered downstream target gene expression of the placental Vitamin D receptor in human idiopathic fetal growth restriction.Crossref | GoogleScholarGoogle Scholar |
Oda, Y., Hu, L. Z., Nguyen, T., Fong, C., Zhang, J., Guo, P., and Bikle, D. D. (2018). Vitamin D receptor is required for proliferation, migration, and differentiation of epidermal stem cells and progeny during cutaneous wound repair. J. Invest. Dermatol. 138, 2423–2431.
| Vitamin D receptor is required for proliferation, migration, and differentiation of epidermal stem cells and progeny during cutaneous wound repair.Crossref | GoogleScholarGoogle Scholar | 29787748PubMed |
Olsson, K., Saini, A., Stromberg, A., Alam, S., Lilja, M., Rullman, E., and Gustafsson, T. (2016). Evidence for vitamin D receptor expression and direct effects of 1alpha,25(OH)2D3 in human skeletal muscle precursor cells. Endocrinology 157, 98–111.
| Evidence for vitamin D receptor expression and direct effects of 1alpha,25(OH)2D3 in human skeletal muscle precursor cells.Crossref | GoogleScholarGoogle Scholar | 26469137PubMed |
Orlando, S., Gallastegui, E., Besson, A., Abril, G., Aligue, R., Pujol, M. J., and Bachs, O. (2015). p27(Kip1) and p21(Cip1) collaborate in the regulation of transcription by recruiting cyclin-Cdk complexes on the promoters of target genes. Nucleic Acids Res. 43, 6860–6873.
| p27(Kip1) and p21(Cip1) collaborate in the regulation of transcription by recruiting cyclin-Cdk complexes on the promoters of target genes.Crossref | GoogleScholarGoogle Scholar | 26071952PubMed |
Parikh, G., Varadinova, M., Suwandhi, P., Araki, T., Rosenwaks, Z., Poretsky, L., and Seto-Young, D. (2010). Vitamin D regulates steroidogenesis and insulin-like growth factor binding protein-1 (IGFBP-1) production in human ovarian cells. Horm. Metab. Res. 42, 754–757.
| Vitamin D regulates steroidogenesis and insulin-like growth factor binding protein-1 (IGFBP-1) production in human ovarian cells.Crossref | GoogleScholarGoogle Scholar | 20711952PubMed |
Pike, J. W., Meyer, M. B., Lee, S. M., Onal, M., and Benkusky, N. A. (2017). The vitamin D receptor: contemporary genomic approaches reveal new basic and translational insights. J. Clin. Invest. 127, 1146–1154.
| The vitamin D receptor: contemporary genomic approaches reveal new basic and translational insights.Crossref | GoogleScholarGoogle Scholar | 28240603PubMed |
Pilz, S., Zittermann, A., Obeid, R., Hahn, A., Pludowski, P., Trummer, C., Lerchbaum, E., Perez-Lopez, F. R., Karras, S. N., and Marz, W. (2018). The role of vitamin D in fertility and during pregnancy and lactation: a review of clinical data. Int. J. Environ. Res. Public Health 15, 2241.
| The role of vitamin D in fertility and during pregnancy and lactation: a review of clinical data.Crossref | GoogleScholarGoogle Scholar |
Pospechova, K., Rozehnal, V., Stejskalova, L., Vrzal, R., Pospisilova, N., Jamborova, G., May, K., Siegmund, W., Dvorak, Z., Nachtigal, P., Semecky, V., and Pavek, P. (2009). Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines. Mol. Cell. Endocrinol. 299, 178–187.
| Expression and activity of vitamin D receptor in the human placenta and in choriocarcinoma BeWo and JEG-3 cell lines.Crossref | GoogleScholarGoogle Scholar | 19133314PubMed |
Rao, A., Coan, A., Welsh, J. E., Barclay, W. W., Koumenis, C., and Cramer, S. D. (2004). Vitamin D receptor and p21/WAF1 are targets of genistein and 1,25-dihydroxyvitamin D-3 in human prostate cancer cells. Cancer Res. 64, 2143–2147.
| Vitamin D receptor and p21/WAF1 are targets of genistein and 1,25-dihydroxyvitamin D-3 in human prostate cancer cells.Crossref | GoogleScholarGoogle Scholar | 15026355PubMed |
Ricca, C., Aillon, A., Bergandi, L., Alotto, D., Castagnoli, C., and Silvagno, F. (2018). Vitamin D receptor is necessary for mitochondrial function and cell health. Int. J. Mol. Sci. 19, 1672–1683.
| Vitamin D receptor is necessary for mitochondrial function and cell health.Crossref | GoogleScholarGoogle Scholar | 29874855PubMed |
Richards, J. S. (2018). From follicular development and ovulation to ovarian cancers: an unexpected journey. Vitam. Horm. 107, 453–472.
| From follicular development and ovulation to ovarian cancers: an unexpected journey.Crossref | GoogleScholarGoogle Scholar | 29544640PubMed |
Sahin, E., Sahin, M. E., Dolanbay, M., Ozcelik, B., Akgun, H., and Saatci, C. (2018). Induction of apoptosis by metformin and progesterone in estrogen-induced endometrial hyperplasia in rats: involvement of the bcl-2 family proteins. Gynecol. Endocrinol. 34, 433–436.
| Induction of apoptosis by metformin and progesterone in estrogen-induced endometrial hyperplasia in rats: involvement of the bcl-2 family proteins.Crossref | GoogleScholarGoogle Scholar | 29179590PubMed |
Samuel, S., and Sitrin, M. D. (2008). Vitamin D’s role in cell proliferation and differentiation. Nutr. Rev. 66, S116–S124.
| Vitamin D’s role in cell proliferation and differentiation.Crossref | GoogleScholarGoogle Scholar | 18844838PubMed |
Saramäki, A., Banwell, C. M., Campbell, M. J., and Carlberg, C. (2006). Regulation of the human p21(waf1/cip1) gene promoter via multiple binding sites for p53 and the vitamin D3 receptor. Nucleic Acids Res. 34, 543–554.
| Regulation of the human p21(waf1/cip1) gene promoter via multiple binding sites for p53 and the vitamin D3 receptor.Crossref | GoogleScholarGoogle Scholar | 16434701PubMed |
Shahbazi, M., Jeddi-Tehrani, M., Zareie, M., Salek-Moghaddam, A., Akhondi, M. M., Bahmanpoor, M., Sadeghi, M. R., and Zarnani, A. H. (2011). Expression profiling of vitamin D receptor in placenta, decidua and ovary of pregnant mice. Placenta 32, 657–664.
| Expression profiling of vitamin D receptor in placenta, decidua and ovary of pregnant mice.Crossref | GoogleScholarGoogle Scholar | 21764449PubMed |
Skorija, K., Cox, M., Sisk, J. M., Dowd, D. R., MacDonald, P. N., Thompson, C. C., and Demay, M. B. (2005). Ligand-independent actions of the vitamin D receptor maintain hair follicle homeostasis. Mol. Endocrinol. 19, 855–862.
| Ligand-independent actions of the vitamin D receptor maintain hair follicle homeostasis.Crossref | GoogleScholarGoogle Scholar | 15591533PubMed |
Skory, R. M., Xu, Y. M., Shea, L. D., and Woodruff, T. K. (2015). Engineering the ovarian cycle using in vitro follicle culture. Hum. Reprod. 30, 1386–1395.
| Engineering the ovarian cycle using in vitro follicle culture.Crossref | GoogleScholarGoogle Scholar | 25784584PubMed |
Smolikova, K., Mlynarcikova, A., and Scsukova, S. (2013). Effect of 1α,25-dihydroxyvitamin D3 on progesterone secretion by porcine ovarian granulosa cells. Endocr. Regul. 47, 123–131.
| Effect of 1α,25-dihydroxyvitamin D3 on progesterone secretion by porcine ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 23889482PubMed |
Stanley, J. A., Lee, J., Nithy, T. K., Arosh, J. A., Burghardt, R. C., and Banu, S. K. (2011). Chromium-VI arrests cell cycle and decreases granulosa cell proliferation by down-regulating cyclin-dependent kinases (CDK) and cyclins and up-regulating CDK-inhibitors. Reprod. Toxicol. 32, 112–123.
| Chromium-VI arrests cell cycle and decreases granulosa cell proliferation by down-regulating cyclin-dependent kinases (CDK) and cyclins and up-regulating CDK-inhibitors.Crossref | GoogleScholarGoogle Scholar | 21621607PubMed |
Suda, T. (2010). What biological functions brought therapeutic effects for skin psoriasis to vitamin D compounds. J. Dermatol. 37, 10.
Tosca, L., Rame, C., Chabrolle, C., Tesseraud, S., and Dupont, J. (2010). Metformin decreases IGF1-induced cell proliferation and protein synthesis through AMP-activated protein kinase in cultured bovine granulosa cells. Reproduction 139, 409–418.
| Metformin decreases IGF1-induced cell proliferation and protein synthesis through AMP-activated protein kinase in cultured bovine granulosa cells.Crossref | GoogleScholarGoogle Scholar | 19906888PubMed |
Verlinden, L., Verstuyf, A., Convents, R., Marcelis, S., Van Camp, M., and Bouillon, R. (1998). Action of 1,25(OH)(2)D-3 on the cell cycle genes, cyclin D1, p21 and p27 in MCF-7 cells. Mol. Cell. Endocrinol. 142, 57–65.
| Action of 1,25(OH)(2)D-3 on the cell cycle genes, cyclin D1, p21 and p27 in MCF-7 cells.Crossref | GoogleScholarGoogle Scholar | 9783903PubMed |
Viganò, P., Lattuada, D., Mangioni, S., Ermellino, L., Vignali, M., Caporizzo, E., Panina-Bordignon, P., Besozzi, M., and Di Blasio, A. M. (2006). Cycling and early pregnant endometrium as a site of regulated expression of the vitamin D system. J. Mol. Endocrinol. 36, 415–424.
| Cycling and early pregnant endometrium as a site of regulated expression of the vitamin D system.Crossref | GoogleScholarGoogle Scholar | 16720713PubMed |
Wirleitner, B., Okhowat, J., Vistejnova, L., Kralickova, M., Karlikova, M., Vanderzwalmen, P., Ectors, F., Hradecky, L., Schuff, M., and Murtinger, M. (2018). Relationship between follicular volume and oocyte competence, blastocyst development and live-birth rate: optimal follicle size for oocyte retrieval. Ultrasound Obstet. Gynecol. 51, 118–125.
| Relationship between follicular volume and oocyte competence, blastocyst development and live-birth rate: optimal follicle size for oocyte retrieval.Crossref | GoogleScholarGoogle Scholar | 29134715PubMed |
Wojtusik, J., and Johnson, P. A. (2012). Vitamin D regulates anti-Müllerian hormone expression in granulosa cells of the hen. Biol. Reprod. 86, 91, 1–7.
| Vitamin D regulates anti-Müllerian hormone expression in granulosa cells of the hen.Crossref | GoogleScholarGoogle Scholar | 22174023PubMed |
Xu, J., Lawson, M. S., Xu, F. H., Du, Y. R., Tkachenko, O. Y., Bishop, C. V., Pejovic-Nezhat, L., Seifer, D. B., and Hennebold, J. D. (2018). Vitamin D3 regulates follicular development and intrafollicular vitamin D biosynthesis and signaling in the primate ovary. Front. Physiol. 9, 1600.
| Vitamin D3 regulates follicular development and intrafollicular vitamin D biosynthesis and signaling in the primate ovary.Crossref | GoogleScholarGoogle Scholar | 30487754PubMed |
Yao, X., Yang, H., Zhang, Y., Ren, C., Nie, H., Fan, Y., Zhou, W., Wang, S., Feng, X., and Wang, F. (2017a). Characterization of GALNTL5 gene sequence and expression in ovine testes and sperm. Theriogenology 95, 54–61.
| Characterization of GALNTL5 gene sequence and expression in ovine testes and sperm.Crossref | GoogleScholarGoogle Scholar | 28460680PubMed |
Yao, X., Zhang, G., Guo, Y., El-Samahy, M., Wang, S., Wan, Y., Han, L., Liu, Z., Wang, F., and Zhang, Y. (2017b). Vitamin D receptor expression and potential role of vitamin D on cell proliferation and steroidogenesis in goat ovarian granulosa cells. Theriogenology 102, 162–173.
| Vitamin D receptor expression and potential role of vitamin D on cell proliferation and steroidogenesis in goat ovarian granulosa cells.Crossref | GoogleScholarGoogle Scholar | 28797922PubMed |
Yao, X., Ei-Samahy, M. A., Fan, L., Zheng, L., Jin, Y., Pang, J., Zhang, G., Liu, Z., and Wang, F. (2018). In vitro influence of selenium on the proliferation of and steroidogenesis in goat luteinized granulosa cells. Theriogenology 114, 70–80.
| In vitro influence of selenium on the proliferation of and steroidogenesis in goat luteinized granulosa cells.Crossref | GoogleScholarGoogle Scholar | 29602134PubMed |
Yoshizawa, T., Handa, Y., Uematsu, Y., Takeda, S., Sekine, K., Yoshihara, Y., Kawakami, T., Arioka, K., Sato, H., Uchiyama, Y., Masushige, S., Fukamizu, A., Matsumoto, T., and Kato, S. (1997). Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat. Genet. 16, 391–396.
| Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning.Crossref | GoogleScholarGoogle Scholar | 9241280PubMed |
Zarnani, A. H., Shahbazi, M., Salek-Moghaddam, A., Zareie, M., Tavakoli, M., Ghasemi, J., Rezania, S., Moravej, A., Torkabadi, E., Rabbani, H., and Jeddi-Tehrani, M. (2010). Vitamin D3 receptor is expressed in the endometrium of cycling mice throughout the estrous cycle. Fertil. Steril. 93, 2738–2743.
| Vitamin D3 receptor is expressed in the endometrium of cycling mice throughout the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 19896660PubMed |
Zhang, Y., Guo, Q., Zhang, Z., Bai, N., Liu, Z., Xiong, M., Wei, Y., Xiang, R., and Tan, X. (2014). VDR status arbitrates the prometastatic effects of tumor-associated macrophages. Mol. Cancer Res. 12, 1181–1191.
| VDR status arbitrates the prometastatic effects of tumor-associated macrophages.Crossref | GoogleScholarGoogle Scholar | 24821711PubMed |
Zhang, G. M., Deng, M. T., Zhang, Y. L., Fan, Y. X., Wan, Y. J., Nie, H. T., Wang, Z. Y., Wang, F., and Lei, Z. H. (2016). Effect of PGC-1alpha overexpression or silencing on mitochondrial apoptosis of goat luteinized granulosa cells. J. Bioenerg. Biomembr. 48, 493–507.
| Effect of PGC-1alpha overexpression or silencing on mitochondrial apoptosis of goat luteinized granulosa cells.Crossref | GoogleScholarGoogle Scholar | 27896503PubMed |
