Spatio-temporal expression patterns of steroidogenic acute regulatory protein (star) during follicular development in the rat ovary

Endocrinology

Volumn 139, Issue 1, 1998, Pages 303-315

  Ronen Fuhrmann, Tamar ^a   Timberg, Rina ^a   King, Steven R ^b   Hales, Karen H ^c   Hales, Dale B ^c   Stocco, Douglas M ^b   Orly, Joseph ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85011519686     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/endo.139.1.5694     Document Type: Article

References (84)

1. Simpson ER, Waterman MR 1988 Regulation of the synthesis of steroidogenic enzymes in adrenal cortical cells by ACTH. Annu Rev Physiol 50:427-440
2. Richards JS, Hedin L 1988 Molecular aspects of hormone action in ovarian follicular development, ovulation, and luteinization. Annu Rev Physiol 50:441-463
3. Hall PF 1986 Cytochromes P-450 and the regulation of steroid synthesis. Steroids 48:133-196
4. Miller WL 1988 Molecular biologv of steroid hormone synthesis. Endocr Rev 9:295-318
5. Stocco DM, Clark BJ 1996 Regulation of the acute production of steroids in steroidogenic cells. Endocr Rev 17:221-244
6. Stocco DM 1997 A StAR search: implications in controlling steroidogenesis. Biol Reprod 56:328-336
7. Stocco DM 1997 The steroidogenic acute regulatory (StAR) protein two year later: an update. Endocrine 6:99-109
8. Privalle CT, Crivello JF, Jefcoate CR 1983 Regulation of intramitochondrial cholesterol transfer to side-chain cleavage cytochrome P450scc in rat adrenal gland. Proc Natl Acad Sci USA 80:702-706
9. Pon LA, Orme-Johnson NR 1988 Acute stimulation of corpus luteum cells by gonadotropin or adenosine 3'5'-monophosphate causes accumulation of a phosphoprotein concurrent with acceleration of steroid synthesis. Endocrinology 123:1942-1948
10. Stocco DM, Sodeman TC1991 The 30-kDa mitochondrial proteins induced by hormone stimulation in MA-10 mouse Leydig tumor cells are processed from larger precursors. J Biol Chem 266:19731-19738
11. Lin D, Sugawara T, Strauss JF, Clark BJ, Stocco DM, Sanger P, Rogol A, Miller WL 1995 Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267:1828-1831
12. Hauffa PT, Miller WL, Grumbach MM, Conte FA, Kaplan SL1985 Congenital adrenal hyperplasia due to deficient cholesterol side-chain cleavage activity (20, 22-desmolase) in a patient treated for 18 years. Clin Endocrinol 23:481-493
13. Clark BJ, Wells J, King SR, Stocco DM 1994 The purification, cloning and expression of a novel LH-induced mitochondrial protein in MA-10 mouse Leydig tumor cells: characterization of the steroidogenic acute regulator protein (StAR). J Biol Chem 269:28314-28322
14. King SR, Ronen-Fuhnnann T, Timberg R, Clark BJ, Orly J, Stocco DM 1995 Steroid production following the in vitro transcription, translation and mitochondrial processing of the protein products of the cDNA for the steroidogenic acute regulatory (StAR) protein. Endocrinology 136:5165-5176
15. Epstein LF, Orme-Johnson NR 1991 Regulation of steroid hormone biosynthesis: identification of precursors of a phosphoprotein targeted to the mitochondrion in stimulated rat adrenal cortex cells. J Biol Chem 266:19739-19745
16. Dohler KD, Wuttke W 1975 Changes in levels of serum gonadotropins, prolactin and gonadal steroids in prepubertal male and female rats. Endocrinology 97:898-907
17. Hsueh AJW, Adashi EY, Jones PBC, Welsh TH 1984 Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev 5:76-126
18. Baird DT 1977 Evidence in vivo for the two-cell hypothesis of oestrogen synthesis by the sheep Graafian follicle. J Reprod FertU 50:183-185
19. Goldring NB, Orly J 1985 Concerted metabolism of steroid hormones produced by co cultured ovarian cell types. J Biol Chem 260:913-921
20. Goldring NB, Farkash Y, Goldschmit D, Orly J 1986 Immunofluorescence probing of the mitochondrial cholesterol side-chain cleavage cytochrome P-450 expressed in differentiating granulosa cells in culture. Endocrinology 119: 2821-2832
21. Goldschmit D, Kraicer P, Orly J 1989 Periovulatory expression of cholesterol side chain cleavage cytochrome P-450 in cumulus cells. Endocrinology 124:369-378
22. Richards JS 1994 Hormonal control of gene expression in the ovarv. Endocr Rev 15:725-751
23. Erickson GF, Wang C, Hsueh AJW 1979 FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 279:336-339
24. Segaloff, Wang H, Richards JS 1990 Hormonal regulation of LH/chronic gonadotropin receptor mRNA in rat ovarian cells during follicular development and luteinization. Mol Endocrinol 4:1856-1865
25. Erickson GF, Magoffin DA, Dyer CA, Hofeditz C 1985 The ovarian androgen producing cells: A review of structure/function relationship. Endocr Rev 6:371
26. Uilenbroek JT, Richards JS 1979 Ovarian follicular development during the rat estrus cycle: gonadotropin receptors and follicular responsiveness. Biol Reprod 20:1159-1165
27. Hsueh AJW, Billig H, Tsafriri A 1994 Ovarian follicular atresia: a hormonally controlled apoptosis process. Endocr Rev 15:707-724
28. Bitzur S, Orly J 1989 Microanalysis of hormone responsive ovarian interstitial gland cells in miniature culture. Endocrinology 124:1471-1484
29. Farkash Y, Timberg R, Orly J 1986 Preparation of antiserum to rat cytochrome P-450 side chain cleavage and its use for ultrastructural localization of the immuno-reactive enzyme by protein A-gold technique. Endocrinology 118: 1353-1365
30. Orly J, Rei Z, Greenberg N, Richards JS 1994 Tyrosine kinase inhibitor AG18 arrests FSH induced granulosa cell differentiation: use of semi-quantitative RT-PCR assay for multiple mRNAs. Endocrinology 134:2336-2346
31. Orly J, Clemens JW, Singer O, Richards JS 1996 Effects of hormones and protein kinase inhibitors on expression of steroidogenic enzyme promoters in electroporated primary rat granulosa cells. Biol Reprod 54:208-218
32. Sandhoff TW, McLean MP 1996 Hormonal regulation of steroidogenic acute regulatory (StAR) protein messenger ribonucleic acid expression in the rat ovary. Endocrine 4:259-267
33. Zor T, Selinger Z 1996 Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal Biochem 236:302-308
34. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680- 685
35. Otter T, King SM, Witman GB 1987 A two-step procedure for efficient electrotransfer of both high-molecular weight (>400, 000) and low-molecular weight (>20, 000) proteins. Anal Biochem 162:370-377
36. Orly J, Sato G, Erickson GF 1980 Serum suppresses the expression of hormonally induced functions in cultured granulosa cells. Cell 20:817-827
37. Gomberg-Malool S, Rei Z, Re'em Y, Posner I, Levitzki A, Orly J 1993 Tyr-phostins inhibit follicle stimulating hormone-mediated functions in cultured rat ovarian granulosa cells. Endocrinology 132:362-370
38. Zlotkin T, Farkash Y, Orly J 1986 Cell specific expression of immunoreactive cholesterol side chain cleavage cytochrome P-450 during follicular development in the ovary. Endocrinology 119:2809-2820
39. Cherradi N, Rossier MF, Vallotton MB, Timberg R, Friedberg I, Orly J, Wang XJ, Stocco DM, Capponi AM 1996 Submitochondrial distribution of three key steroidogenic proteins (steroidogenic acute regulatory protein, P450 side-chain cleavage and 3β-hydroxysteroid dehydrogenase isomerase enzymes) upon stimulation by intracellular calcium in adrenal glomerulosa cells. J Biol Chem 272:7899-7907
40. Camp TA, Rahal JO, Mayo KE 1991 Cellular localization and hormonal regulation of follicle stimulating hormone and luteinizing hormone receptor messenger RNAs in the rat ovary. Mol Endocrinol 5:1405-1417
41. Chan Y-L, Lin A, McNally J, Peleg D, Meyuhus O, Wool IG1987 The primary structure of rat ribosomal protein L19. J Biol Chem 262:1111-1115
42. Butcher RL, Collins WE, Fugo NW 1974 Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17β throughout the 4-day estrus cycle of the rat. Endocrinology 94:1704-1708
43. Richards JS 1980 Maturation of ovarian follicles: actions and interactions of pituitary and ovarian hormones of follicular cell differentiation. Physiol Rev 60:51-89
44. Abraham GE, Odell WD, Swerdloff RS 1972 Simultaneous radioimmunoassay of plasma FSH, LH, progesterone, 17β-hydroxy progesterone and estradiol-17β during the menstrual cycle. J Clin Endocrinol Metab 34:312-318
45. Orly J 1989 Orchestrated expression of steroidogenic side-chain cleavage cytochrome P450 during follicular development in the rat ovary. J Reprod Fert [Suppl] 37:155-162
46. Hickey GJ, Chen S, Besman MJ, Shively JE, Hall PF, Gaddy-Kurten D, Richards JS 1988 Hormonal regulation, tissue distribution, and content of aromatase cytochrome P450 messenger ribonucleic acid and enzyme in rat ovarian follicles and corpora lutea: relationship to estradiol biosynthesis. Endocrinology 122:1426-1436
47. Miller WL 1988 Molecular biologv of steroid hormone synthesis. Endocr Rev 9:295-318
48. Simpson ER, MacDonald PC 1981 Endocrine physiology of the placenta. Annu Rev Physiol 43:163-188
49. Simpson ER, McCarthy JL, Peterson JA1978 Evidence that the cycloheximide-sensitive site of adrenocorticotropic hormone action is in the mitochondrion: changes in pregnenolone formation, cholesterol content, and the electron paramagnetic resonance spectra of cytochrome P-450. J Biol Chem 253:3135-3139
50. Stocco DM, Clark BJ 1996 Role of the steroidogenic acute regulatory protein (StAR) in steroidogenesis. Biochem Pharmacol 51:197-205
51. Stocco DM 1997 A StAR search: implications in controlling steroidogenesis. Biol Reprod 56:328-336
52. Hanukoglu I, Hanukoglu Z 1986 Stoichiometry of mitochondrial cytochrome P450, adrenodoxin and adrenodoxin reductase in adrenal cortex and corpus luteum. Eur J Biochem 157:27-31
53. Miller WL, Tyrrell JB 1995 The adrenal cortex. In: Felig P, Baxter J, Frohman L (eds) Endocrinology and Metabolism. McGraw Hill, New York, pp 555-711
54. Gallagher TF, Yoshida K, Roffwarg HD 1973 ACTH and cortisol secretory patterns in man. J Clin Endocrinol Metab 36:1058
55. Parker Jr CR, Costoff A, Muldoon TG, Mahesh VB 1976 Actions of pregnant mare serum gonadotropin in the immature female rat: correlative changes in blood steroids, gonadotropins, and cytoplasmic estradiol receptors of the anterior pituitary and hypothalamus. Endocrinology 98:129-138
56. Erickson GF, Wang C, Hsueh AJW 1979 FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 279:336-339
57. Daniel SAJ, Armstrong DT 1980 Enhancement of follicle-stimulating hor-mone-induced aromatase activity by androgens in cultured rat granulosa cells. Endocrinology 107:1027-1033
58. Hillier SG, De Zwart FA 1981 Evidence that granulosa cell aromatase induction/activation by follicle stimulating hormone is an androgen receptor-regulated process in vitro. Endocrinology 109:1303-1305
59. Fitzpatrick SL, Richards JS 1991 Regulation of cytochrome P450 aromatase messenger ribonucleic acid and activity by steroids and gonadotropins in rat granulosa cells. Endocrinology 129:1452-1462
60. Richards JS, Bogovich K 1987 Effects of human chorionic gonadotropin and progesterone on follicular development in the immature rat. Endocrinology 111:1429-1438
61. Bogovich K, Richards JS, Reichert Jr LE 1981 Obligatory role of luteinizing hormone (LH) in the initiating of preovulatory follicular growth in the pregnant rat: specific effects of human chorionic gonadotropin and follicle stimulating hormone on LH receptors and steroidogenesis in theca, granulosa and luteal cells. Endocrinology 109:860-867
62. Boggaram V, Zuber MX, Waterman MR 1984 Turnover of newly synthesized cytochromes P450scc, P450 lib and adrenodoxin in bovine adrenocortical cells in monolavers culture: effect of adrenocorticotropin. Arch Biochem Biophys 23:518-524
63. Garren LD, Ney RL, Davis WW 1965 Studies on the role of protein synthesis in the regulation of corticosterone production by adrenocorticotropic hormone in vivo. Proc Natl Acad Sci USA 53:1443-1451
64. Vemikos-Danellis J, Hall M 1965 Inhibition of adrenocortical responsiveness to ACTH by actinomycin D in vivo. Nature 207:766
65. Clark BJ, Soo S-C, Caron KM, Ikeda Y, Parker KL, Stocco DM 1995 Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol Endocrinol 9:1346-1355
66. Kiriakidou M, McAllister JM, Sugawara T, Strauss III JF 1996 Expression of steroidogenic acute regulatory protein (StAR) in the human ovary. J Clin Endocrinol Metab 81:4122-4128
67. Juengel JL, Meberg BM, Turzillo AM, Nett TM, Niswender GD 1995 Hormonal regulation of messenger ribonucleic acid encoding steroidogenic acute regulatory protein in ovine corpora lutea. Endocrinology 136:5423-5429
68. Soumano K, Price CA 1997 Ovarian follicular steroidogenic acute regulator protein, low density lipoprotein receptor, and cytochrome P450 side chain cleavage messenger ribonucleic acids in cattle undergoing superovulation. Biol Reprod 56:516-522
69. Smith MS, Freeman ME, Neill JD 1975 The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the Rat: Prolactin, Gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96:219-227
70. Tsafriri A, Braw RH 1984 Experimental approaches to atresia in mammals. Oxford Rev Reprod Biol 6:226.45
71. Dahl E 1971 Studies of the fine structure of ovarian interstitial tissue. J Anat 108:275
72. Taya K, Saidapur SK, Greenwald GS 1980 Interstitium: Site of steroid synthesis in the ovary of the long term hypophysectomized hamster. Biol Reprod 22:307
73. Carithers JR 1976 Ultrastructure of rat ovarian interstitial cells: Response to luteinizing hormone. J Ultrastruct Res 55:96
74. Park OK, Mayo KE 1991 Transient expression of progesterone receptor messenger RNA in ovarian granulosa cells after the preovulatory luteinizing hormone surge. Mol Endocrinol 5:967-978
75. Oonk RB, Krasnow JS, Beattie WG, Richards JS 1989 1989 Cyclic AMP-dependent and independent regulation of cholesterol side-chain cleavage P450 (P450scc) in rat ovarian granulosa cells and corpora lutea. J Biol Chem 264:21934-21942
76. Richards JS, Hedin L, Caston L 1986 Differentiation of rat ovarian theca cells: evidence for functional luteinization. Endocrinology 118:1660-1668
77. Weiss M, Eckstein B 1984 Periovulatory changes in steroid C17, 20-lyase activity in ovaries of immature rats treated with pregnant mare serum gonadotropin. Endocrinology 114:1912-1916
78. Natraj U, Richards JS 1993 Hormonal regulation, localization and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinolgy 133:761-769
79. Hartung S, Rust W, Balvers M, Ivell R 1995 Molecular cloning and the in vivo expression of the bovine steroidogenic acute regulatory protein. Biochem Biophys Res Commun 215:649-653
80. Pescador N, Soumano K, Stocco DM, Price CA, Murphy BD 1996 Steroidogenic Acute Regulator protein in bovine corpora lutea. Biol Reprod 55:485-491
81. Sandhoff TW, McLean MP 1996 Prostaglandin F2a reduces steroidogenic acute regulatory (StAR) protein messenger ribonucleic acid expression in the rat ovary. Endocrine 5:183-190
82. Ferguson JJ 1963 Protein synthesis and adrenocorticotropin responsiveness. J Biol Chem 238:2754-2759
83. Schulster D, Richardson MC, Palfreyman JW 1974 The role of protein synthesis in adrenocorticotrophin action: effect of cycloheximide and puromycin on the steroidogenic response of isolated adrenocortical cells. Mol Cell Endocrinol 2:17-29
84. Stevens VL, Xu T, Lambeth JD 1993 Cholesterol trafficking in steroidogenic cells: reversible cycloheximide-dependent accumulation of cholesterol in a pre-steroidogenic pool. Eur J Biochem 216:557-563