1,25-Dihydroxyvitamin D3 increases testosterone-induced 17beta-estradiol secretion and reverses testosterone-reduced connexin 43 in rat granulosa cells

Reproductive Biology and Endocrinology

Volumn 12, Issue 1, 2014, Pages

  Lee, Ching Tien ^a   Wang, Jiz Yuh ^b   Chou, Kuang Yi ^c   Hsu, Ming I ^d  

^a HSIN SHENG COLLEGE OF MEDICAL CARE AND MANAGEMENT   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL TAIPEI UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

1,25 dihydroxyvitamin D3; 17beta estradiol; Calcium; Connexin 43; Estrogenesis; Granulosa cells; Polycystic ovary syndrome; Testosterone

Indexed keywords

AROMATASE; CALCITRIOL; CONNEXIN 43; ESTRADIOL; ESTRADIOL RECEPTOR; MESSENGER RNA; NIFEDIPINE; TESTOSTERONE; ANTIESTROGEN; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHELATING AGENT; CONNEXIN 43 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL COMMUNICATION; CELL CULTURE; CELL JUNCTION; CELL LYSATE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ESTROGEN RELEASE; FEMALE; GRANULOSA CELL; IMMUNOCYTOCHEMISTRY; NONHUMAN; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIOIMMUNOASSAY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CALCIUM SIGNALING; CHEMISTRY; CYTOLOGY; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOSPHORYLATION; PROTEIN PROCESSING; SECRETION (PROCESS); SPRAGUE DAWLEY RAT; UPREGULATION;

RATTUS;

ANIMALS; AROMATASE; CALCITRIOL; CALCIUM CHANNEL BLOCKERS; CALCIUM CHELATING AGENTS; CALCIUM SIGNALING; CELLS, CULTURED; CONNEXIN 43; DOWN-REGULATION; ESTRADIOL; ESTROGEN ANTAGONISTS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GRANULOSA CELLS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTRADIOL; TESTOSTERONE; UP-REGULATION;

EID: 84907261001     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-12-90     Document Type: Article

References (50)

1. Ryan KJ. Biochemistry of aromatase: significance to female reproductive physiology. Cancer Res 1982, 42:3342s-3344s.
2. Luo W, Wiltbank MC. Distinct regulation by steroids of messenger RNAs for FSHR and CYP19A1 in bovine granulosa cells. Biol Reprod 2006, 75:217-225. 10.1095/biolreprod.105.047407, 16641147.
3. Belin F, Goudet G, Duchamp G, Gerard N. Intrafollicular concentrations of steroids and steroidogenic enzymes in relation to follicular development in the mare. Biol Reprod 2000, 62:1335-1343. 10.1095/biolreprod62.5.1335, 10775185.
4. Stocco C. Aromatase expression in the ovary: hormonal and molecular regulation. Steroids 2008, 73:473-487. 10.1016/j.steroids.2008.01.017, 2365984, 18321551.
5. Otala M, Makinen S, Tuuri T, Sjoberg J, Pentikainen V, Matikainen T, Dunkel L. Effects of testosterone, dihydrotestosterone, and 17beta-estradiol on human ovarian tissue survival in culture. Fertil Steril 2004, 82(Suppl 3):1077-1085.
6. Vendola KA, Zhou J, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest 1998, 101:2622-2629. 10.1172/JCI2081, 508852, 9637695.
7. Murray AA, Gosden RG, Allison V, Spears N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil 1998, 113:27-33. 10.1530/jrf.0.1130027, 9713373.
8. Hu YC, Wang PH, Yeh S, Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY, Chang C. Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci U S A 2004, 101:11209-11214. 10.1073/pnas.0404372101, 509185, 15277682.
9. Hamel M, Vanselow J, Nicola ES, Price CA. Androstenedione increases cytochrome P450 aromatase messenger ribonucleic acid transcripts in nonluteinizing bovine granulosa cells. Mol Reprod Dev 2005, 70:175-183. 10.1002/mrd.20194, 15570613.
10. Wu YG, Bennett J, Talla D, Stocco C. Testosterone, not 5alpha-dihydrotestosterone, stimulates LRH-1 leading to FSH-independent expression of Cyp19 and P450scc in granulosa cells. Mol Endocrinol 2011, 25:656-668. 10.1210/me.2010-0367, 3063088, 21273442.
11. Hsu MI, Liou TH, Chou SY, Chang CY, Hsu CS. Diagnostic criteria for polycystic ovary syndrome in Taiwanese Chinese women: comparison between Rotterdam 2003 and NIH 1990. Fertil Steril 2007, 88:727-729. 10.1016/j.fertnstert.2006.11.149, 17706215.
12. Wehr E, Pilz S, Schweighofer N, Giuliani A, Kopera D, Pieber TR, Obermayer-Pietsch B. Association of hypovitaminosis D with metabolic disturbances in polycystic ovary syndrome. Eur J Endocrinol 2009, 161:575-582. 10.1530/EJE-09-0432, 19628650.
13. Wehr E, Trummer O, Giuliani A, Gruber HJ, Pieber TR, Obermayer-Pietsch B. Vitamin D-associated polymorphisms are related to insulin resistance and vitamin D deficiency in polycystic ovary syndrome. Eur J Endocrinol 2011, 164:741-749. 10.1530/EJE-11-0134, 21389086.
14. Lerchbaum E, Obermayer-Pietsch B. Vitamin D and fertility: a systematic review. Eur J Endocrinol 2012, 166:765-778. 10.1530/EJE-11-0984, 22275473.
15. Johnson JA, Grande JP, Roche PC, Kumar R. Immunohistochemical detection and distribution of the 1,25-dihydroxyvitamin D3 receptor in rat reproductive tissues. Histochem Cell Biol 1996, 105:7-15. 10.1007/BF01450873, 8824901.
16. Kinuta K, Tanaka H, Moriwake T, Aya K, Kato S, Seino Y. Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology 2000, 141:1317-1324.
17. Boland R, Buitrago C, De Boland AR. Modulation of tyrosine phosphorylation signalling pathways by 1alpha,25(OH)2-vitamin D3. Trends Endocrinol Metab 2005, 16:280-287. 10.1016/j.tem.2005.06.003, 16002300.
18. Buitrago C, Vazquez G, De Boland AR, Boland RL. Activation of Src kinase in skeletal muscle cells by 1, 1,25-(OH(2))-vitamin D(3) correlates with tyrosine phosphorylation of the vitamin D receptor (VDR) and VDR-Src interaction. J Cell Biochem 2000, 79:274-281. 10.1002/1097-4644(20001101)79:2<274::AID-JCB100>3.0.CO;2-R, 10967554.
19. Buitrago C, Vazquez G, De Boland AR, Boland R. The vitamin D receptor mediates rapid changes in muscle protein tyrosine phosphorylation induced by 1,25(OH)(2)D(3). Biochem Biophys Res Commun 2001, 289:1150-1156. 10.1006/bbrc.2001.6072, 11741312.
20. Catalano S, Barone I, Giordano C, Rizza P, Qi H, Gu G, Malivindi R, Bonofiglio D, Ando S. Rapid estradiol/ERalpha signaling enhances aromatase enzymatic activity in breast cancer cells. Mol Endocrinol 2009, 23:1634-1645. 10.1210/me.2009-0039, 19556341.
21. Cheng J, Watkins SC, Walker WH. Testosterone activates mitogen-activated protein kinase via Src kinase and the epidermal growth factor receptor in sertoli cells. Endocrinology 2007, 148:2066-2074. 10.1210/en.2006-1465, 17272394.
22. Kidder GM, Mhawi AA. Gap junctions and ovarian folliculogenesis. Reproduction 2002, 123:613-620. 10.1530/rep.0.1230613, 12006089.
23. Teilmann SC. Differential expression and localisation of connexin-37 and connexin-43 in follicles of different stages in the 4-week-old mouse ovary. Mol Cell Endocrinol 2005, 234:27-35. 10.1016/j.mce.2004.10.014, 15836950.
24. Ackert CL, Gittens JE, O'Brien MJ, Eppig JJ, Kidder GM. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 2001, 233:258-270. 10.1006/dbio.2001.0216, 11336494.
25. Wu CH, Yang JG, Yang JJ, Lin YM, Tsai HD, Lin CY, Kuo PL. Androgen excess down-regulates connexin43 in a human granulosa cell line. Fertil Steril 2010, 94:2938-2941. 10.1016/j.fertnstert.2010.06.077, 20684953.
26. Clairmont A, Tessman D, Stock A, Nicolai S, Stahl W, Sies H. Induction of gap junctional intercellular communication by vitamin D in human skin fibroblasts is dependent on the nuclear Induction of gap junctional intercellular communication by vitamin D in human skin fibroblasts is dependent on the nuclear vitamin D receptor. Carcinogenesis 1996, 17:1389-1391. 10.1093/carcin/17.6.1389, 8681462.
27. Ke FC, Fang SH, Lee MT, Sheu SY, Lai SY, Chen YJ, Huang FL, Wang PS, Stocco DM, Hwang JJ. Lindane, a gap junction blocker, suppresses FSH and transforming growth factor beta1-induced connexin43 gap junction formation and steroidogenesis in rat granulosa cells. J Endocrinol 2005, 184:555-566. 10.1677/joe.1.05776, 15749814.
28. Merhi Z, Doswell A, Krebs K, Cipolla M. Vitamin D alters genes involved in follicular development and steroidogenesis in human cumulus granulosa cells. J Clin Endocrinol Metab 2014, 99:E1137-1145. 10.1210/jc.2013-4161, 24628555.
29. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63. 10.1016/0022-1759(83)90303-4, 6606682.
30. Teissier MP, Chable H, Paulhac S, Aubard Y. Comparison of follicle steroidogenesis from normal and polycystic ovaries in women undergoing IVF: relationship between steroid concentrations, follicle size, oocyte quality and fecundability. Hum Reprod 2000, 15:2471-2477. 10.1093/humrep/15.12.2471, 11098013.
31. Eilso Nielsen M, Rasmussen IA, Fukuda M, Westergaard LG, Yding Andersen C. Concentrations of anti-Mullerian hormone in fluid from small human antral follicles show a negative correlation with CYP19 mRNA expression in the corresponding granulosa cells. Mol Hum Reprod 2010, 16:637-643. 10.1093/molehr/gaq001, 20064870.
32. Lundqvist J, Norlin M, Wikvall K. 1alpha,25-Dihydroxyvitamin D3 exerts tissue-specific effects on estrogen and androgen metabolism. Biochim Biophys Acta 1811, 2011:263-270.
33. Krishnan AV, Swami S, Peng L, Wang J, Moreno J, Feldman D. Tissue-selective regulation of aromatase expression by calcitriol: implications for breast cancer therapy. Endocrinology 2010, 151:32-42. 10.1210/en.2009-0855, 2803154, 19906814.
34. Enjuanes A, Garcia-Giralt N, Supervia A, Nogues X, Ruiz-Gaspa S, Bustamante M, Mellibovsky L, Grinberg D, Balcells S, Diez-Perez A. Functional analysis of the I.3, I.6, pII and I.4 promoters of CYP19 (aromatase) gene in human osteoblasts and their role in vitamin D and dexamethasone stimulation. Eur J Endocrinol 2005, 153:981-988. 10.1530/eje.1.02032, 16322405.
35. Barrera D, Avila E, Hernandez G, Halhali A, Biruete B, Larrea F, Diaz L. Estradiol and progesterone synthesis in human placenta is stimulated by calcitriol. J Steroid Biochem Mol Biol 2007, 103:529-532. 10.1016/j.jsbmb.2006.12.097, 17257826.
36. Lundqvist J, Hansen SK, Lykkesfeldt AE. Vitamin D analog EB1089 inhibits aromatase expression by dissociation of comodulator WSTF from the CYP19A1 promoter-a new regulatory pathway for aromatase. Biochim Biophys Acta 1833, 2013:40-47.
37. Ting HJ, Bao BY, Hsu CL, Lee YF. Androgen-receptor coregulators mediate the suppressive effect of androgen signals on vitamin D receptor activity. Endocrine 2005, 26:1-9. 10.1385/ENDO:26:1:001, 15805579.
38. Miller TW, Shin I, Kagawa N, Evans DB, Waterman MR, Arteaga CL. Aromatase is phosphorylated in situ at serine-118. J Steroid Biochem Mol Biol 2008, 112:95-101. 10.1016/j.jsbmb.2008.09.001, 2856845, 18822378.
39. Barone I, Giordano C, Malivindi R, Lanzino M, Rizza P, Casaburi I, Bonofiglio D, Catalano S, Ando S. Estrogens and PTP1B function in a novel pathway to regulate aromatase enzymatic activity in breast cancer cells. Endocrinology 2012, 153:5157-5166. 10.1210/en.2012-1561, 22962253.
40. Christakos S, Dhawan P, Porta A, Mady LJ, Seth T. Vitamin D and intestinal calcium absorption. Mol Cell Endocrinol 2011, 347:25-29. 10.1016/j.mce.2011.05.038, 3405161, 21664413.
41. Agoston A, Kunz L, Krieger A, Mayerhofer A. Two types of calcium channels in human ovarian endocrine cells: involvement in steroidogenesis. J Clin Endocrinol Metab 2004, 89:4503-4512. 10.1210/jc.2003-032219, 15356055.
42. Paul S, Kundu S, Pramanick K, Bandyopadhyay A, Mukherjee D. Regulation of ovarian steroidogenesis in vitro by gonadotropin in common carp Cyprinus carpio: interaction between calcium- and adenylate cyclase-dependent pathways and involvement of ERK signaling cascade. J Mol Endocrinol 2010, 45:207-218. 10.1677/JME-10-0061, 20668068.
43. Weitzel JM, Vernunft A, Kruger B, Plinski C, Viergutz T. LOX-1 regulates estrogenesis via intracellular calcium release from bovine granulosa cells. Cytometry A 2014, 85:88-93. 10.1002/cyto.a.22353, 24115745.
44. Reilly CM, Cannady WE, Mahesh VB, Stopper VS, De Sevilla LM, Mills TM. Duration of estrogen exposure prior to follicle-stimulating hormone stimulation is critical to granulosa cell growth and differentiation in rats. Biol Reprod 1996, 54:1336-1342. 10.1095/biolreprod54.6.1336, 8724362.
45. Emmen JM, Couse JF, Elmore SA, Yates MM, Kissling GE, Korach KS. In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER){alpha} and ER{beta} null mice indicate a role for ER{beta} in follicular maturation. Endocrinology 2005, 146:2817-2826. 10.1210/en.2004-1108, 15731357.
46. Gougeon A. Human ovarian follicular development: from activation of resting follicles to preovulatory maturation. Ann Endocrinol (Paris) 2010, 71:132-143. 10.1016/j.ando.2010.02.021, 20362973.
47. Matsuda F, Inoue N, Manabe N, Ohkura S. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J Reprod Dev 2012, 58:44-50. 10.1262/jrd.2011-012, 22450284.
48. Kinuta K. Regulation of vitamin D biosynthesis by calcium. Clin Calcium 2003, 13:899-903.
49. Wojtusik J, Johnson PA. Vitamin D regulates anti-Mullerian hormone expression in granulosa cells of the hen. Biol Reprod 2012, 86:91. 10.1095/biolreprod.111.094110, 22174023.
50. Irani M, Merhi Z. Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review. Fertil Steril 2014, 102:460-468. e463, 10.1016/j.fertnstert.2014.04.046, 24933120.