The potential function of steroid sulphalase in steroid production and steroidogenic acute regulatory protein

Biochemical Journal

Volumn 380, Issue 1, 2004, Pages 153-160

  Sugawara, Teruo ^a   Fujimoto, Seiichiro ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cholesterol sulphate (CS); MLN64; Steroid hormone; Steroid sulphatase (STS); Steroidogenic acute regulatory protein (StAR protein)

Indexed keywords

BIOSYNTHESIS; ENZYMES; GENES; HORMONES; TISSUE;

BLOT ANALYSIS; TRANSCRIPTION-TRANSLATION REACTIONS;

BIOCHEMISTRY;

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); PREGNENOLONE; STEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STERYL SULFATASE;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; GENE EXPRESSION; HORMONE SYNTHESIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; STEROIDOGENESIS; WESTERN BLOTTING;

ANIMALS; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; COS CELLS; GENE EXPRESSION REGULATION; HALF-LIFE; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; PHOSPHOPROTEINS; PREGNENOLONE; PROTEIN PRECURSORS; RECOMBINANT FUSION PROTEINS; STEROIDS; STERYL-SULFATASE; TRANSFECTION;

ANIMALIA; MAMMALIA; VECTORS;

EID: 2642566808     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031379     Document Type: Article

References (55)

1. Stocco, D. M. and Clark, B. J. (1996) Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17, 221-244
2. Clark, B. J., Wells, J., King, S. R. and Stocco, D. M. (1994) The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells: characterization of the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 269, 28314-28322
3. Lin, D., Sugawara, T., Strauss, III, J. F., Clark, B. J., Stocco, D. M., Saenger, P., Rogol, A. and Miller, W. L. (1995) Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267, 1828-1831
4. Adessi, G. L., Nhuan, T. Q. and Vingler, P. (1982) In vivo and in vitro metabolism of estrone and estradiol-17β and their 3-sulfates in pregnant female guinea pigs: a plausible prehormone role of estrogen-sulfates in the maternal uterus. J. Steroid Biochem. 16, 107-116
5. Choe, B. K., Lillehoj, H. S., Dong, M. K., Gleason, S., Barron, M. and Rose, N. R. (1982) Characterization of antigenic sites of human prostatic acid phosphatase. Ann. N.Y. Acad. Sci. 390, 16-26
6. Martel, C., Melner, M. H., Gagne, D., Simard, J. and Labrie, F. (1994) Widespread tissue distribution of steroid sulfatase, 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase (3β-HSD), 17β-HSD 5 α-reductase and aromatase activities in the rhesus monkey. Mol. Cell. Endocrinol. 104, 103-111
7. Sugawara, T., Holt, J. A., Driscoll, D., Strauss, III, J. F., Lin, D., Miller, W. L., Patterson, D., Clancy, K. P., Hart, I. M., Clark, B. J. et al. (1995) Human steroidogenic acute regulatory protein: functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13. Proc. Natl. Acad. Sci. U.S.A. 92, 4778-4782
8. Arakane, F., King, S. R., Du, Y., Kallen, C. B., Walsh, L. P., Watari, H., Stocco, D. M. and Strauss, III, J. F. (1997) Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J. Biol. Chem. 272, 32656-32662
9. Moog-Lutz, C., Tomasetto, C., Regnier, C. H., Wendung, C., Lutz, Y., Muller, D., Chenard, M. P., Basset, P. and Rio, M. C. (1997) MLN64 exhibits homology with the steroidogenic acute regulatory protein (STAR) and is over-expressed in human breast carcinomas. Int. J. Cancer 71, 183-191
10. Clemens, J. W., Kabler, H. L., Sarap, J. L., Beyer, A. R., Li, P. K. and Selcer, K. W. (2000) Steroid sulfatase activity in the rat ovary, cultured granulosa cells, and a granulosa cell line. J. Steroid Biochem. Mol. Biol. 75, 245-252
11. Strauss, III, J. F., Kallen, C. B., Christenson, L. K., Watari, H., Devoto, L., Arakane, F., Kiriakidou, M. and Sugawara, T. (1999) The steroidogenic acute regulatory protein (StAR): a window into the complexities of intracellular cholesterol trafficking. Recent Prog. Horm. Res. 54, 369-394
12. Harikrishna, J. A., Black, S. M., Szklarz, G. D. and Miller, W. L. (1993) Construction and function of fusion enzymes of the human cytochrome P450scc system. DNA Cell Biol. 12, 371-379
13. Watari, H., Arakane, F., Moog-Lutz, C., Kallen, C. B., Tomasetto, C., Gerton, G. L., Rio, M. C., Baker, M. E. and Strauss, III, J. F (1997) MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. Proc. Natl. Acad. Sci. U.S.A. 94, 8462-8467
14. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685
15. Sugawara, T., Honke, K., Gasa, S., Tanaka, T., Fujimoto, S. and Makita, A. (1994) Serum levels of steroid sulfatase protein in gynecologic carcinomas. Clin. Chim. Acta 226, 13-20
16. Sugawara, T., Shimizu, H., Hoshi, N., Fujimoto, Y., Nakajima, A. and Fujimoto, S. (2000) PCR diagnosis of X-linked ichthyosis: identification of a novel mutation (E560P) of the steroid sulfatase gene. Hum. Mutat. 15, 296
17. Toaff, M. E., Strauss, III, J. F., Flickinger, G. L. and Shattil, S. J. (1979) Relationship of cholesterol supply to luteal mitochondrial steroid synthesis. J. Biol. Chem. 254, 3977-3982
18. Privalle, C. T., Crivello, J. F. and Jefcoate, C. R. (1983) Regulation of intramitochondrial cholesterol transfer to side-chain cleavage cytochrome P-450 in rat adrenal gland. Proc. Natl. Acad. Sci. U.S.A. 80, 702-706
19. Stein, C., Hille, A., Seidel, J., Rijnbout, S., Waheed, A., Schmidt, B., Geuze, H. and von Figura, K. (1989) Cloning and expression of human steroid-sulfatase: membrane topology, glycosylation, and subcellular distribution in BHK-21 cells. J. Biol. Chem. 264, 13865-13872
20. Jacobs, N. L., Andemariam, B., Underwood, K. W., Panchalingam, K., Sternberg, D., Kielian, M. and Liscum, L. (1997) Analysis of a Chinese hamster ovary cell mutant with defective mobilization of cholesterol from the plasma membrane to the endoplasmic reticulum. J. Lipid Res. 38, 1973-1987
21. Xu, X. X. and Lambeth, J. D. (1989) Cholesterol sulfate is a naturally occurring inhibitor of steroidogenesis in isolated rat adrenal mitochondria. J. Biol. Chem. 264, 7222-7227
22. Lambeth, J. D., Xu, X. X. and Glover, M. (1987) Cholesterol sulfate inhibits adrenal mitochondrial cholesterol side chain cleavage at a site distinct from cytochrome P-450scc: evidence for an intramitochondrial cholesterol translocator. J. Biol. Chem. 262, 9181-9188
23. Petrescu, A. D., Gallegos, A. M., Okamura, Y., Strauss, III, J. F. and Schroeder, F (2001) Steroidogenic acute regulatory protein binds cholesterol and modulates mitochondrial membrane sterol domain dynamics. J. Biol. Chem. 276, 36970-36982
24. Alpy, F., Stoeckel, M. E., Dierich, A., Escola, J. M., Wendling, C., Chenard, M. P., Vanier, M. T., Gruenberg, J., Tomasetto, C. and Rio, M. C. (2001) The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J. Biol. Chem. 276, 4261-4269
25. Ponting, C. P. and Aravind, L. (1999) START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24, 130-132
26. Bose, H. S., Whittal, R. M., Huang, M. C., Baldwin, M. A. and Miller, W. L. (2000) N-218 MLN64, a protein with StAR-like steroidogenic activity, is folded and cleaved similarly to StAR. Biochemistry 39, 11722-11731
27. Tsujishita, Y. and Hurley, J. H. (2000) Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Biol. 7, 408-414
28. Bose, H. S., Whittal, R. M., Baldwin, M. A. and Miller, W. L. (1999) The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule. Proc. Natl. Acad. Sci. U.S.A. 96, 7250-7255
29. Christensen, K., Bose, H. S., Harris, F. M., Miller, W. L. and Bell, J. D. (2001) Binding of steroidogenic acute regulatory protein to synthetic membranes suggests an active molten globule. J. Biol. Chem. 276, 17044-17051
30. Stocco, D. M. and Chen, W. (1991) Presence of identical mitochondrial proteins in unstimulated constitutive steroid-producing R2C rat Leydig tumor and stimulated nonconstitutive steroid-producing MA-10 mouse Leydig tumor cells. Endocrinology 128, 1918-1926
31. Rao, R. M., Jo, Y., Leers-Sucheta, S, Bose, H. S., Miller, W. L., Azhar, S. and Stocco, D. M. (2003) Differential regulation of steroid hormone biosynthesis in R2C and MA-10 Leydig tumor cells: role of SR-B1-mediated selective cholesteryl ester transport. Biol. Reprod. 68, 114-121
32. Christenson, L. K., McAllister, J. M., Martin, K. O., Javitt, N. B., Osborne, T. F. and Strauss, III, J. F. (1998) Oxysterol regulation of steroidogenic acute regulatory protein gene expression. Structural specificity and transcriptional and posttranscriptional actions. J. Biol. Chem. 273, 30729-30735
33. Sugawara, T., Lin, D., Holt, J. A., Martin, K. O., Javitt, N. B., Miller, W. L. and Strauss, III, J. F. (1995) Structure of the human steroidogenic acute regulatory protein (StAR) gene: StAR stimulates mitochondrial cholesterol 27-hydroxylase activity. Biochemistry 34, 12506-12512
34. Arakane, F., Kallen, C. B., Watari, H., Foster, J. A., Sepuri, N. B., Pain, D., Stayrook, S. E., Lewis, M., Gerton, G. L. and Strauss, III, J. F. (1998) The mechanism of action of steroidogenic acute regulatory protein (StAR): StAR acts on the outside of mitochondria to stimulate steroidogenesis. J. Biol. Chem. 273, 16339-16345
35. Tuckey, R. C., Headlam, M. J., Bose, H. S. and Miller, W. L. (2002) Transfer of cholesterol between phospholipid vesicles mediated by the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 277, 47123-47128
36. Artemenko, I. P., Zhao, D., Hales, D. B., Hales, K. H. and Jefcoate, C. R. (2001) Mitochondrial processing of newly synthesized steroidogenic acute regulatory protein (StAR), but not total StAR, mediates cholesterol transfer to cytochrome P450 side chain cleavage enzyme in adrenal cells. J. Biol. Chem. 276, 46583-46596
37. Bose, H., Lingappa, V. R. and Miller, W. L. (2002) Rapid regulation of steroidogenesis by mitochondrial protein import. Nature (London) 417, 87-91
38. Epstein, L. F. and Orme-Johnson, N. R. (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
39. Jefcoate, C. (2002) High-flux mitochondrial cholesterol trafficking, a specialized function of the adrenal cortex. J. Clin. Invest. 110, 881-890
40. Zolotarjova, N. I., Hollis, G. F. and Wynn, R. (2001) Unusually stable and long-lived ligand-induced conformations of integrins. J. Biol. Chem. 276, 17063-17068
41. Dowell, P., Peterson, V. J., Zabriskie, T. M. and Leid, M. (1997) Ligand-induced peroxisome proliferator-activated receptor α conformational change. J. Biol. Chem. 272, 2013-2020
42. Hirotani, M., Tsukamoto, T., Bourdeaux, J., Sadano, H. and Osumi, T. (2001) Stabilization of peroxisome proliferator-activated receptor α by the ligand. Biochem. Biophys. Res. Commun. 288, 106-110
43. Ishii, T., Hasegawa, T., Pai, C. I., Yvgi-Ohana, N., Timberg, R., Zhao, L., Majdic, G., Chung, B. C., Orly, J. and Parker, K. L. (2002) The roles of circulating high-density lipoproteins and trophic hormones in the phenotype of knockout mice lacking the steroidogenic acute regulatory protein. Mol. Endocrinol. 16, 2297-2309
44. Bose, H. S., Sugawara, T., Strauss, III, J. F. and Miller, W. L. (1996) The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. N. Engl. J. Med. 335, 1870-1878
45. Papadopoulos, V. (1993) Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr. Rev. 14, 222-240
46. Chanderbhan, R. F., Kharroubi, A. T., Noland, B. J., Scallen, T. J. and Vahouny, G. V. (1986) Sterol carrier protein 2: further evidence for its role in adrenal steroidogenesis. Endocr. Res. 12, 351-370
47. Yamamoto, R., Kallen, C.B., Babalola, G. O., Rennert, H., Billheimer, J. T. and Strauss, III, J. F. (1991) Cloning and expression of a cDNA encoding human sterol carrier protein 2. Proc. Natl. Acad. Sci. U.S.A. 88, 463-467
48. Zhang, M., Liu, P., Dwyer, N. K., Christenson, L. K., Fujimoto, T., Martinez, F., Comly, M., Hanover, J. A., Blanchette-Mackie, E. J. and Strauss, III, J. F. (2002) MLN64 mediates mobilization of lysosomal cholesterol to steroidogenic mitochondria. J. Biol. Chem. 277, 33300-33310
49. Christenson, L. K., Johnson, P. F., McAllister, J. M. and Strauss, III, J. F. (1999) CCAAT/enhancer-binding proteins regulate expression of the human steroidogenic acute regulatory protein (StAR) gene. J. Biol. Chem. 274, 26591-26598
50. Reinhart, A. J., Williams, S. C., Clark, B. J. and Stocco, D. M. (1999) SF-1 (steroidogenic factor-1) and C/EBP β (CCAAT/enhancer binding protein-β) cooperate to regulate the murine StAR (steroidogenic acute regulatory) promoter. Mol. Endocrinol. 13, 729-741
51. Wooton-Kee, C. R. and Clark, B. J. (2000) Steroidogenic factor-1 influences protein-deoxyribonucleic acid interactions within the cyclic adenosine 3,5-monophosphate-responsive regions of the murine steroidogenic acute regulatory protein gene. Endocrinology 141, 1345-1355
52. Takemori, H., Katoh, Y., Horike, N., Doi, J. and Okamoto, M. (2002) ACTH-induced nucleocytoplasmic translocation of salt-inducible kinase: implication in the protein kinase A-activated gene transcription in mouse adrenocortical tumor cells. J. Biol. Chem. 277, 42334-42343
53. Christenson, L. K., Osborne, T. F., McAllister, J. M. and Strauss, III, J. F. (2001) Conditional response of the human steroidogenic acute regulatory protein gene promoter to sterol regulatory element binding protein-1a. Endocrinology 142, 28-36
54. Brown, M. S. and Goldstein, J. L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331-340
55. Yokoyama, C., Wang, X., Briggs, M. R., Admon, A., Wu, J., Hua, X., Goldstein, J. L. and Brown, M. S. (1993) SREBP-1, a basic-helix-loop-helix- leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 75, 187-197