Differential regulation of steroid hormone biosynthesis in R2C and MA-10 Leydig tumor cells: Role of SR-B1-mediated selective cholesteryl ester transport

Biology of Reproduction

Volumn 68, Issue 1, 2003, Pages 114-121

  Rao, Rekha M ^a   Jo, Youngah ^a   Leers Sucheta, Susan ^b   Bose, Himangshu S ^c   Miller, Walter L ^c   Azhar, Salman ^b   Stocco, Douglas M ^a  

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

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cyclic adenosine monophosphate; Leydig cells; Progesterone; Steroid hormones; Testis

Indexed keywords

CHOLESTEROL; CHOLESTEROL ESTER; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOCHROME P450; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; PREGNENOLONE; PROGESTERONE; RNA; SCAVENGER RECEPTOR; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRIACYLGLYCEROL LIPASE;

ANIMAL CELL; ARTICLE; BIOSYNTHESIS; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; LEYDIG CELL; MALE; MITOCHONDRIAL MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONTENT; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD36; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; BUCLADESINE; CHOLESTEROL; CHOLESTEROL ESTERASE; CHOLESTEROL ESTERS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION; LEYDIG CELL TUMOR; MALE; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; PHOSPHOPROTEINS; RATS; RECEPTORS, IMMUNOLOGIC; RECEPTORS, LIPOPROTEIN; RECEPTORS, SCAVENGER; RNA, MESSENGER; SCAVENGER RECEPTORS, CLASS B; STEROIDS; TESTICULAR NEOPLASMS; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0037230367     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.102.007518     Document Type: Article

References (50)

1. Ascoli M, Puett D. Gonadotropin binding and stimulation of steroidogenesis in Leydig tumor cells. Proc Natl Acad Sci U S A 1978; 75:99-102.
2. Clark BJ, Wells J, King SR, Stocco DM. 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 1994; 269:28314-28322.
3. Stocco DM. Tracking the role of a StAR in the sky of the new millennium. Mol Endocrinol 2001; 15:1245-1254.
4. Lin D, Sugawara T, Strauss III JF, Clark BJ, Stocco DM, Saenger P, Rogol A, Miller WL. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 1995; 267:1828-1831.
5. Christenson LK, Strauss III JF. Steroidogenic acute regulatory protein (StAR) and the intramitochondrial translocation of cholesterol. Biochim Biophys Acta 2000; 1529:175-187.
6. Shin S, Yasumura, Y, Sato GH. Studies on interstitial cells in tissue culture. II. Steroid biosynthesis by a clonal line of rat testicular interstitial cells. Endocrinology 1968; 82:614-616.
7. Freeman DA. Constitutive steroidogenesis in the R2C Leydig tumor cell line is maintained by the adenosine 3′,5′-cyclic monophosphate-independent production of a cycloheximide-sensitive factor that enhances mitochondrial pregnenolone biosynthesis. Endocrinology 1987; 120:124-132.
8. Stocco DM, Chen W. 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 1991; 128:1918-1926.
9. King SR, Ronen-Fuhrmann T, Timberg R, Clark BJ, Orly J, Stocco DM. Steroid production after in vitro transcription, translation, and mitochondrial processing of protein products of complementary deoxyribonucleic acid for steroidogenic acute regulatory protein. Endocrinology 1995; 136:5165-5176.
10. Gwynne JT. Strauss III JF. The role of lipoproteins in steroidogenesis and cholesterol metabolism in steroidogenic glands. Endocr Rev 1982; 3:299-329.
11. Pedersen RC. Cholesterol biosynthesis, storage, and mobilization in steroidogenic organs. In: Yeagle PL (ed.), Biology of Cholesterol. Boca Raton, FL: CRC Press Inc.; 1988: 39-69.
12. Reaven E, Tsai L, Azhar S. Cholesterol uptake by the "selective" pathway of ovarian granulose cells: Early intracellular events. J Lipid Res 1995; 36:1602-1617.
13. Hui DA. Molecular biology of enzymes involved with cholesteryl ester hydrolysis in mammalian tissues. Biochim Biophys Acta 1996; 1303:1-14.
14. Glass C, Pittman RC, Weinstein DB, Steinberg D. Dissociation of tissue uptake of cholesteryl ester from that of apoprotein A-1 of rat plasma high density lipoprotein: Selective delivery of cholesteryl ester to liver, adrenal, and gonad. Proc Natl Acad U S A 1983; 80:5435-5439.
15. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science 1986; 232:34-47.
16. Pittman RC, Knecht TP, Rosenbaum MS, Taylor CA. A nonendocytic mechanism for the selective uptake of high density lipoprotein-associated cholesterol esters. J Biol Chem 1987; 262:2443-2450.
17. Reaven E, Tsai L, Azhar S. Intracellular events in the "selective" transport of lipoprotein-derived cholesteryl esters. J Biol Chem 1996; 271:16208-16217.
18. Krieger M. Charting the fate of the "good cholesterol": Identification and characterization of the high-density lipoprotein receptor SR-BI. Annu Rev Biochem 1999; 68:523-558.
19. Williams DL, Connelly MA, Temel RE, Swarnakar S, Phillips MC, de la Llera-Moya M, Rothblat GH. Scavenger receptor BI and cholesterol trafficking. Curr Opin Lipidol 1999; 10:329-339.
20. Silver DL, Tall AR. The cellular biology of scavenger receptor class B type 1. Curr Opin Lipidol 2001; 12:497-504.
21. Azhar S, Nomoto A, Leers-Sucheta S, Reaven E. Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model. J Lipid Res 1998; 39:1616-1628.
22. Clark BJ, Soo SC, Caron KM, Ikeda Y, Parker KL, Stocco DM. Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol Endocrinol 1995; 9:1346-1355.
23. Bose HS, Whittal RM, Baldwin MA, Miller WL. The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule. Proc Natl Acad Sci U S A 1999; 96:7250-7255.
24. Reaven E, Leers-Sucheta S, Nomoto A, Azhar S. Expression of scavenger receptor class B type 1 (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system. Proc Natl Acad Sci U S A 2001; 98:1613-1618.
25. Morimoto C, Kameda K, Tsujita T, Okuda H. Relationships between lipolysis induced by various lipolytic agents and hormone-sensitive lipase in rat fat cells. J Lipid Res 2001; 42:120-127.
26. Jokinen EV, Landschulz KT, Wyne KL, Ho YK, Frykman PK, Hobbs HH. Regulation of the very low density lipoprotein receptor by thyroid hormone in rat skeletal muscle. J Biol Chem 1994; 269:26411-26418.
27. Wang X, Dyson MT, Mondillo C, Patrignani Z, Pignataro O, Stocco DM. Interaction between arachidonic acid and cAMP signaling pathways enhances steroidogenesis and StAR expression in MA-10 Leydig tumor cells. Mol Cell Endocrinol 2002; 188:55-63.
28. Wang X, Walsh LP, Reinhart AJ, Stocco DM. The role of arachidonic acid in steroidogenesis and steroidogenic acute regulatory (StAR) gene and protein expression. J BioI Chem 2000; 275:20204-20209.
29. Bose HS, Whittal RM, Huang MC, Baldwin MA, Miller WL. N-218 MLN64, a protein with StAR-like steroidogenic activity, is folded and cleaved similarly to StAR. Biochemistry 2000; 39:11722-11731.
30. Arakane F, Sugawara T, Nishino H, Liu Z, Holt JA, Pain D, Stocco DM, Miller WL, Strauss III JF. Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: Implications for the mechanism of StAR action. Proc Natl Acad Sci U S A 1996; 93:13731-13736.
31. Bose HS, Baldwin MA, Miller WL. Incorrect folding of steroidogenic acute regulatory protein (StAR) in congenital lipoid adrenal hyperplasia. Biochemistry 1998; 37:9768-9775.
32. Reaven E, Shi XY, Azhar S. Interaction of lipoproteins with isolated ovary plasma membranes. J Biol Chem 1990; 265:19100-19111.
33. Azhar S, Tsai L, Reaven E. Uptake and utilization of lipoprotein cholesteryl esters by rat granulosa cells. Biochim Biophys Acta 1990; 1047:148-160.
34. Azhar S, Stewart D, Reaven E. Utilization of cholesterol-rich lipoproteins by perfused rat adrenals. J Lipid Res 1989; 30:1799-1810.
35. Markwell MAK, Hass SM, Bieber LL, Tolbert NE. A modification of the Lowry procedure to simplify protein determination in membranes and lipoprotein fractions. Anal Biochem 1987; 87:206-210.
36. Popplewell PY, Azhar S. Effects of aging on cholesterol content and cholesterol metabolizing enzymes in rat adrenal gland. Endocrinology 1987; 121:64-73.
37. Freeman DA. Plasma membrane cholesterol: Removal and insertion into the membrane and utilization as substrate for steroidogenesis. Endocrinology 1989; 124:2527-2534.
38. Tercyak AM. Determination of cholesterol and cholesterol esters. J Nutr Biochem 1991; 2:281-292.
39. Stocco DM, Clark BJ. Regulation of the acute production of steroids in steroidogenic cells. Endocr Rev 1996; 17:221-244.
40. Stocco DM. StAR protein and regulation of steroid hormone biosynthesis. Annu Rev Physiol 2001; 63:193-213.
41. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs HH. Regulation of scavenger receptor, class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J Clin Invest 1996; 98:984-995.
42. Reaven E, Nomoto A, Leers-Sucheta S, Temel R, Williams DL, Azhar S. Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian model. Endocrinology 1998; 139:2847-2856.
43. Reaven E, Spicher M, Azhar S. Microvillar channels: A unique plasma membrane compartment for concentrating lipoproteins on the surface of rat adrenal cortical cells. J Lipid Res 1989; 30:1551-1560.
44. Clark BJ, Ranganathan V, Combs R. Post-translational regulation of steroidogenic acute regulatory protein by cAMP-dependent protein kinase A. Endocr Res 2000; 26:681-689.
45. Engh RA, Girod A, Kinzel V, Huber R, Bossemeyer D. Crystal structures of catalytic subunit of cAMP-dependent protein kinase complex with isoquinolinesulfonyl protein kinase inhibitors H7, H8 and H89. Structural implications for selectivity. J Biol Chem 1996; 271:26157-26164.
46. Lopez D, Sandhoff TW, McLean MP. Steroidogenic factor-1 mediates cyclic 3′,5′-adenosine monophosphate regulation of the high density lipoprotein receptor. Endocrinology 1999; 140:3034-3044.
47. Manna PR, Dyson MT, Eubank DW, Clark BJ, Lalli E, Sussone-Corsi P, Zeleznik AJ, Stocco DM. Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol Endocrinol 2002; 16: 184-199.
48. Manna PR, Roy P, Clark BJ, Stocco DM, Huhtaniemi IT. Interaction of thyroid hormone and steroidogenic acute regulatory (StAR) protein in the regulation of murine Leydig cell steroidogenesis. J Steroid Biochem Mol Biol 2001; 76:167-177.
49. Wang X, Stocco DM. Cyclic AMP and arachidonic acid: A tale of two pathways. Mol Cell Endocrinol 1999; 158:7-12.
50. Richards JS. New signaling pathways for hormones and cyclic adenosine 3′,5′-monophosphate action in endocrine cells. Mol Endocrinol 2001; 15:209-218.