Molecular pathology and mechanism of action of the steroidogenic acute regulatory protein, STAR

Journal of Steroid Biochemistry and Molecular Biology

Volumn 69, Issue 1-6, 1999, Pages 131-141

  Miller, Walter L ^a   Strauss III, Jerome F ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

17 HYDROXYCORTICOSTEROID; 17 OXOSTEROID; CHOLESTEROL; COMPLEMENTARY DNA; CORTICOSTEROID; CORTICOTROPIN; CYCLIC AMP; CYTOCHROME P450; GONADOTROPIN; PREGNENOLONE; PROGESTERONE; REGULATOR PROTEIN; STEROID 21 MONOOXYGENASE; STEROID HORMONE; TESTOSTERONE; VITAMIN D;

CARBOXY TERMINAL SEQUENCE; CLINICAL FEATURE; CONFERENCE PAPER; CONGENITAL ADRENAL HYPERPLASIA; GENE MUTATION; GENETIC TRANSCRIPTION; GENOTYPE; HUMAN; INFRARED SPECTROSCOPY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; STEROIDOGENESIS; STRUCTURE ACTIVITY RELATION;

ADRENAL HYPERPLASIA, CONGENITAL; ANIMALS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; GENOTYPE; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PHOSPHOPROTEINS;

EID: 0033051733     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-0760(98)00153-8     Document Type: Conference Paper

References (70)

1. Moore C.C.D., Miller W.L. The role of transcriptional regulation in steroid hormone biosynthesis. J. Steroid. Biochem. Mol. Biol. 40:1991;517-525.
2. Hum D.W., Miller W.L. Transcriptional regulation of human genes for steroidogenic enzymes. Clin. Chem. 39:1993;333-340.
3. Stocco D.M., Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17:1996;221-244.
4. Clark B.J., Stocco D.M. Steroidogenic acute regulatory protein: the StAR still shines brightly. Mol. Cell Endocr. 134:1997;1-8.
5. Lin D., Sugawara T., Strauss J.F. III, Clark B.J., Stocco D.M., Saenger P., Rogol A., Miller W.L. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science. 267:1995;1828-1831.
6. Miller W.L. Congenital lipoid adrenal hyperplasia: the human gene knockout of the steroidogenic acute regulatory protein. J. Mol. Endocrinol. 17:1997;227-240.
7. Miller W.L. Lessons from congenital lipoid adrenal hyperplasia. Curr. Opin. Endocr. Diab. 5:1998;155-161.
8. Chung B., Matteson K.J., Voutilainen R., Mohandas T.K., Miller W.L. Human cholesterol side-chain cleavage enzyme, P450scc: cDNA cloning, assignment of the gene to chromosome 15, and expression in the placenta. Proc. Natl. Acad. Sci. U.S.A. 83:1986;8962-8966.
9. Morohashi K., Sogawa K., Omura T., Fujii-Kuriyama Y. Gene structure of human cytochrome P-450(scc), cholesterol desmolase. J. Biochem. 101:1987;879-887.
10. Sparkes R.S., Klisak I., Miller W.L. Regional mapping of genes encoding human steroidogenic enzymes: P450scc to 15q23-q24, adrenodoxin to 11q22; adrenodoxin reductase to 17q24-q25; and P450c17 to 10q24-q25. DNA Cell Biol. 10:1991;359-365.
11. Miller W.L. Molecular biology of steroid hormone synthesis. Endocr. Rev. 9:1988;295-318.
12. Picado-Leonard J., Voutilainen R., Kao L., Chung B., Strauss J.F. III, Miller W.L. Human adrenodoxin: cloning of three cDNAs and cycloheximide enhancement in JEG-3 cells. J. Biol. Chem. 263:1988;3240-3244. corrected 11016.
13. Solish S.B., Picado-Leonard J., Morel Y., Kuhn R.W., Mohandas T.K., Hanukoglu I., Miller W.L. Human adrenodoxin reductase: two mRNAs encoded by a single gene of chromosome 17cen→q25 are expressed in steroidogenic tissues. Proc. Natl. Acad. Sci. U.S.A. 71:1988;7104-7108.
14. Chang C.-Y., Wu D.-A., Lai C.-C., Miller W.L., Chung B. Cloning and structure of the human adrenodoxin gene. DNA. 7:1988;609-615.
15. Lin D., Shi Y., Miller W.L. Cloning and sequence of the human adrenodoxin reductase gene. Proc. Natl. Acad. Sci. U.S.A. 87:1990;8516-8520.
16. Fardella C.E., Miller W.L. Molecular biology of mineralocorticoid metabolism. Ann. Rev. Nutrition. 16:1996;443-470.
17. 3-25-hydroxylase activity. Biochem. J. 320:1996;267-271.
18. Fu G.K., Lin D., Zhang M.Y.H., Bikle D.D., Shackleton C.H.L., Miller W.L., Portale A.A. Cloning of human 25-hydroxy vitamin D-1α-hydroxylase and mutations causing vitamin D-dependant rickets type I. Mol. Endocrinol. 11:1997;1961-1970.
19. Fu G.K., Portale A.A., Miller W.L. Complete structure of the human gene for the vitamin D 1α-hydroxyase, P450c1α DNA Cell Biol. 16:1997;1499-1507.
20. Black S.M., Harikrishna J.A., Szklarz G.D., Miller W.L. The mitochondrial environment is required for activity of the cholesterol side-chain cleavage enzyme, cytochrome P450scc. Proc. Natl. Acad. Sci. U.S.A. 91:1994;7247-7251.
21. Stone D., Hechter O. Studies on ACTH action in perfused bovine adrenals: aspects of progesterone as an intermediary in cortico-steroidogenesis. Arch. Biochem. Biophys. 54:1955;121-128.
22. Ferguson J.J. Protein synthesis and adrenocorticotropin responsiveness. J. Biol. Chem. 238:1963;2754-2759.
23. Garren L.D., Ney R.L., Davis W.W. Studies on the role of protein synthesis in the regulation of corticosterone production by adrenocorticotropic hormone in vivo. Proc. Natl. Acad. Sci. U.S.A. 53:1965;1443-1450.
24. Garren L.D., Davis W.W., Crocco R.M. Puromycin analogs: action of adrenocorticotropic hormone and the role of glycogen. Science. 152:1966;1386-1388.
25. Pon L.A., Orme-Johnson N.R. Acute stimulation of steroidogenesis in corpus luteum and adrenal cortex by peptide hormones. J. Biol. Chem. 261:1986;6594-6599.
26. Epstein L.F., Orme-Johnson N.R. Regulation of steroid hormone biosynthesis: identification of precursors of a phosphoprotein targeted to the mitochondrion in stimulated rat adrenal cortex cells. J. Biol. Chem. 266:1991;19739-19745.
27. Stocco D.M., Sodeman T.C. The 30 kDa mitochondrial protein induced by hormone stimulation in MA-10 mouse Leydig tumor cells are processed from larger precursors. J. Biol. Chem. 266:1991;19731-19738.
28. Clark B.J., Wells J., King S.R., Stocco D.M. The purification, cloning and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 cells mouse Leydig tumor cells: characterization of the steroidogenic acute regulatory protein (StAR). J. Biol. Chem. 269:1994;28314-28322.
29. Kirkland R.T., Kirkland J.L., Johnson C.M., Horning M.G., Librik L., Clayton G.W. Congenital lipoid adrenal hyperplasia in an 8-year old phenotypic female. J. Clin. Endocrinol. Metab. 36:1973;488-496.
30. Hauffa B.P., Miller W.L., Grumbach M.M., Conte F.A., Kaplan S.L. Congenital adrenal hyperplasia due to deficient cholesterol side-chain cleavage activity (20,22 desmolase) in a patient treated for 18 years. Clin. Endocrinol. 23:1985;481-493.
31. Camacho A.M., Kowarski A., Migeon C.J., Brough A. Congenital adrenal hyperplasia due to a deficiency of one of the enzymes involved in the biosynthesis of pregnenolone. J. Clin. Endocrinol. Metab. 28:1968;153-161.
32. Degenhart H.J., Visser K.H.A., Boon H., O'Doherty N.J.D. Evidence for deficiency of 20α cholesterol hydroxylase activity in adrenal tissue of a patient with lipoid adrenal hyperplasia. Acta Endocrinologia. 71:1972;512-518.
33. Koizumi S., Kyoya S., Miyawaki T., Kidani H., Funabashi T., Nakashima H., Nakanuma Y., Ohta G., Itagaki E., Katagiri M. Cholesterol side-chain cleavage enzyme activity and cytochrome P450 content in adrenal mitochondria of a patient with congenital lipoid adrenal hyperplasia (Prader disease). Clin. Chim. Acta. 77:1977;301-306.
34. Matteson K.J., Chung B., Urdea M.S., Miller W.L. Study of cholesterol side chain cleavage (20,22 desmolase) deficiency causing congenital lipoid adrenal hyperplasia using bovine-sequence P450scc oligodeoxyribonucleotide probes. Endocrinology. 118:1986;1296-1305.
35. Lin D., Gitelman S.E., Saenger P., Miller W.L. Normal genes for the cholesterol side chain cleavage enzyme, P450scc, in congenital lipoid adrenal hyperplasia. J. Clin. Invest. 88:1991;1955-1962.
36. Sakai Y., Yanase T., Okabe Y., Hara T., Waterman M., Takayanagi R., Haji M., Nawata H. No mutation in cytochrome P450 side chain cleavage in a patient with congenital lipoid adrenal hyperplasia. J. Clin. Endocrinol. Metab. 79:1994;1198-1201.
37. Fukami M., Sato S., Ogata T., Matsuo N. Lack of mutations in P450scc gene (CYP11A) in six Japanese patients with congenital lipoid adrenal hyperplasia. Clin. Pediatr. Endocrinol. 4:1995;39-46.
38. Okuyama E., Nishi N., Onishi S., Itoh S., Ishii Y., Miyanaka H., Fujita K., Ichikawa Y. A novel splicing junction mutation in the gene for the steroidogenic acute regulatory protein causes congenital lipoid adrenal hyperplasia. J. Clin. Endocrinol. Metab. 82:1997;2337-2342.
39. Saenger P., Klonari Z., Black S.M., Compagnone N., Mellon S.H., Fleischer A., Abrams C.A.L., Shackleton C.H.L., Miller W.L. Prenatal diagnosis of congenital lipoid adrenal hyperplasia. J. Clin. Endocrinol. Metab. 80:1995;200-205.
40. Miller W.L. Why nobody has P450scc (20,22 desmolase) deficiency (letter). J. Clin. Endocrinol. Metab. 83:1998;1399-1400.
41. Toaff M.E., Schleyer H., Strauss J.F. III Metabolism of 25-hydroxycholesterol by rat luteal mitochondria and dispersed cells. Endocrinology. 111:1982;1785-1790.
42. Bose H.S., Sugawara T., Strauss J.F. III, Miller W.L. The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. New Engl. J. Med. 335:1996;1870-1878.
43. Harikrishna J.A., Black S.M., Szklarz G.D., Miller W.L. Construction and function of fusion enzymes of the human cytochrome P450scc system. DNA Cell Biol. 12:1993;371-379.
44. Sugawara T., Holt J.A., Driscoll D., Strauss J.F. III, Lin D., Miller W.L., Patterson D., Clancy K.P., Hart I.M., Clark B.J., Stocco D.M. Human steroidogenic acute regulatory protein (StAR): functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and an expressed pseudogene to chromosome 13. Proc. Natl. Acad. Sci. U.S.A. 92:1995;4778-4782.
45. Tee M.K., Lin D., Sugawara T., Holt J.A., Guiguen Y., Buckingham B., Strauss J.F. III, Miller W.L. T→A transversion 11 bp from a splice acceptor site in the gene for steroidogenic acute regulatory protein causes congenital lipoid adrenal hyperplasia. Hum. Mol. Genet. 4:1995;2299-2305.
46. Bose H.S., Pescovitz O.H., Miller W.L. Spontaneous feminization in a 46,XX female patient with congenital lipoid adrenal hyperplasia caused by a homozygous frame-shift mutation in the steroidogenic acute regulatory protein. J. Clin. Endocrinol. Metab. 82:1997;1511-1515.
47. Nakae J., Tajima T., Sugawara T., Arakane F., Hanaki K., Hotsubo T., Igarashi N., Igarashi Y., Ishii T., Koda N., Kondo T., Kohno H., Nakagawa Y., Tachibana K., Takeshima Y., Tsubouchi K., Strauss J.F. III, Fujieda K. Analysis of the steroidogenic acute regulatory protein (StAR) gene in Japanese patients with congenital lipoid adrenal hyerplasia. Hum. Mol. Genet. 6:1997;571-576.
48. Mellon S.H. Neurosteroids: biochemistry, modes of action and clinical relevance. J. Clin. Endocrinol. Metab. 78:1994;1003-1008.
49. Pollack S.E., Furth E.E., Kallen C.B., Arakane F., Kiriakidou M., Kozarsky K.F., Strauss J.F. III Localization of steroidogenic acute regulatory protein in human tissues. J. Clin. Endocrinol. Metab. 82:1997;4243-4251.
50. Watari H., Arakane F., Moog-Lutz C., Callen C.B., Tomasetto C., Gerton G.L., Rio M.C., Baker M.E., Strauss J.F. III MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. Proc. Natl. Acad. Sci. U.S.A. 94:1997;8462-8467.
51. Yang X., Iwamoto K., Wang M., Artwohl J., Mason J.I., Pang S. Inherited congenital adrenal hyperplasia in the rabbit is caused by a deletion in the gene encoding cytochrome P450 cholesterol side-chain cleavage enzyme. Endocrinology. 132:1993;1977-1982.
52. Miller W.L. Mitochondrial specificity of the early steps in steroidogenesis. J. Steroid. Biochem. Mol. Biol. 55:1995;607-616.
53. Tanae A., Miki Y., Hibi I. Pubertal presentation in patients with congenital lipoid adrenal hyperplasia (Prader's syndrome). Acta Pædiatr. Jpn. 30(Suppl):1988;236-238.
54. Matsuo N., Tsuzaki S., Anzo M., Ogata T., Sato S. The phenotypic definition of congenital lipoid adrenal hyperplasia: analysis of the 67 Japanese patients (abstract). Horm. Res. 41(suppl):1994;106. (Abstract).
55. Cole T.J., Blendy J.A., Monaghan A.P., Krieglstein K., Schmid W., Aguzzi A., Fantuzzi G., Hummler E., Unsicker K., Schutz G. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severly retards lung maturation. Genes. Dev. 9:1995;1608-1621.
56. Fujieda K., Tajima T., Nakae J., Sageshima S., Tachibana K., Suwa S., Sugawara T., Strauss J.F. III Spontaneous puberty in 46,XX subjects with congenital lipoid adrenal hypreplasia. J. Clin. Invest. 99:1997;1265-1271.
57. Katsumata N., Tanae A., Shinagawa T., Nagashima-Miyokawa A., Shimizu M., Yasunaga T., Tanaka T., Hibi I. Detection of the missense mutation A218V in the steroidogenic acute regulatory protein gene of a Japanese patient with congenital lipoid adrenal hyperplasia. Clin. Pediatr. Endocrinol. 6:1997;33-37.
58. H.-W. Yoo, G.-H. Kim, Molecular and clinical characterization of Korean patients with congenital lipoid adrenal hyperplasia. J. Ped. Endocrinol. Metab. (in press).
59. Bose H.S., Baldwin M.A., Miller W.L. Incorrect folding of steroidogenic acute regulatory protein (StAR) in congenital lipoid adrenal hyperplasia. Biochemistry. 37:1998;9768-9775.
60. Voutilainen R., Miller W.L. Developmental expression of genes for the steroidogenic enzymes P450scc (20,22 desmolase), P450c17 (17α-hydroxylase/17,20 lyase) and P450c21 (21-hydroxylase) in the human fetus. J. Clin. Endocrinol. Metab. 63:1986;1145-1150.
61. Kiriakidou M., McAllister J.M., Sugawara T., Strauss J.F. III Expression of steroidogenic acute regulatory protein (StAR) in the human ovary. J. Clin. Endocrinol. Metab. 81:1996;4122-4128.
62. Caron K., Soo S.-C., Wetsel W., Stocco D., Clark B., Parker K. Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia. Proc. Natl. Acad. Sci. U.S.A. 94:1997;11540-11545.
63. Arakane F., Sugawara T., Nishino H., Liu Z., Holt J.A., Pain D., Stocco D.M., Miller W.L., Strauss J.F. III Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial targeting sequence: implications for the mechanism of StAR action. Proc. Natl. Acad. Sci. U.S.A. 93:1996;13731-13736.
64. Arakane F., Kallen C.B., Watari H., Foster J.A., Sepuri N.B.V., Pain D., Stayrook S.E., Lewis M., Gerton G.L., Strauss J.F. III The mechanism of action of steroidogenic acute regulatory protein (StAR): StAR acts on the outside of mitochondria to stimulate steroidogenesis. J. Biol. Chem. 273:1998;16339-16345.
65. Papadopoulos V. Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr. Rev. 14:1993;222-240.
66. Amri H., Ogwuegbu S.O., Boujrad N., Drieu K., Papadopoulos V. In vivo regulation of peripheral-type benzodiazepine receptor and glucocorticoid synthesis by Ginkgo biloba extract EGb 761 and isolated ginkgolides. Endocrinology. 137:1996;5707-5718.
67. Papadopoulos V., Amri H., Boujrad N., Cascio C., Culty M., Garnier M., Hardwick M., Li H., Vidic B., Brown A.S., Reversa J.L., Bernassau J.M., Drieu K. Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids. 62:1997;21-28.
68. Papadopoulos V., Amri H., Li H., Boujrad N., Vidic B., Garnier M. Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J. Biol. Chem. 272:1997;32129-32135.
69. Arakane F., King S.R., Du Y., Kallen C.B., Walsh L.P., Watari H., Stocco D.M., Strauss J.F. III Phosphorylation of steroidogenic acute regulatory protein (StAR) modules its steroidogenic activity. J. Biol. Chem. 272:1997;32656-32662.
70. Sugawara T., Lin D., Holt J.A., Martin K.O., Javitt N.B., Miller W.L., Strauss J.F. III The structure of the human steroidogenic acute regulatory (StAR) protein gene: StAR stimulates mitochondrial cholesterol 27-hydroxylase activity. Biochemistry. 34:1995;12506-12512.