The differential regulation of steroidogenic acute regulatory protein-mediated steroidogenesis by type I and type II PKA in MA-10 cells

Molecular and Cellular Endocrinology

Volumn 300, Issue 1-2, 2009, Pages 94-103

  Dyson, Matthew T ^a   Kowalewski, Mariusz P ^a   Manna, Pulak R ^a   Stocco, Douglas M ^a  

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

Author keywords

cAMP; cAMP dependent protein kinase; Leydig; PKA; STAR; Steroidogenesis

Indexed keywords

CHOLESTEROL; CYCLIC AMP DEPENDENT PROTEIN KINASE 1; CYCLIC AMP DEPENDENT PROTEIN KINASE 2; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSCRIPTION FACTOR JUNB;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CHOLESTEROL TRANSPORT; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION; INTRACELLULAR TRANSPORT; LEYDIG CELL TUMOR; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; STEROIDOGENESIS; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE, TUMOR; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASE TYPE I; CYCLIC AMP-DEPENDENT PROTEIN KINASE TYPE II; ENZYME ACTIVATION; ISOENZYMES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LEYDIG CELL TUMOR; MICE; PHOSPHOPROTEINS; STEROIDS;

EID: 59649089523     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.11.029     Document Type: Article

References (67)

1. Arakane F., King S.R., Du Y., Kallen C.B., Walsh L.P., Watari H., Stocco D.M., and Strauss III J.F. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J. Biol. Chem. 272 (1997) 32656-32662
2. Ariyoshi N., Kim Y.C., Artemenko I., Bhattacharyya K.K., and Jefcoate C.R. Characterization of the rat Star gene that encodes the predominant 3.5-kilobase pair mRNA. ACTH stimulation of adrenal steroids in vivo precedes elevation of Star mRNA and protein. J. Biol. Chem. 273 (1998) 7610-7619
3. Belfrage P., Fredrikson G., Nilsson N.O., and Stralfors P. Regulation of adipose-tissue lipolysis by phosphorylation of hormone-sensitive lipase. Int. J. Obes. 5 (1981) 635-641
4. Bose H., Lingappa V.R., and Miller W.L. Rapid regulation of steroidogenesis by mitochondrial protein import. Nature 417 (2002) 87-91
5. Carlson C.R., Lygren B., Berge T., Hoshi N., Wong W., Tasken K., and Scott J.D. Delineation of type I protein kinase A-selective signaling events using an RI anchoring disruptor. J. Biol. Chem. 281 (2006) 21535-21545
6. Caron K.M., Ikeda Y., Soo S.C., Stocco D.M., Parker K.L., and Clark B.J. Characterization of the promoter region of the mouse gene encoding the steroidogenic acute regulatory protein. Mol. Endocrinol. 11 (1997) 138-147
7. Chaudhary L.R., and Stocco D.M. Stimulation of progesterone production by phorbol-12-myristate-13-acetate in MA-10 Leydig tumor cells. Biochimie 70 (1988) 1353-1360
8. Chin K.V., Yang W.L., Ravatn R., Kita T., Reitman E., Vettori D., Cvijic M.E., Shin M., and Iacono L. Reinventing the wheel of cyclic AMP: novel mechanisms of cAMP signaling. Ann. N.Y. Acad. Sci. 968 (2002) 49-64
9. Christensen A.E., Selheim F., de Rooij J., Dremier S., Schwede F., Dao K.K., Martinez A., Maenhaut C., Bos J.L., Genieser H.G., and Doskeland S.O. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J. Biol. Chem. 278 (2003) 35394-35402
10. Clark B.J., Soo S.C., Caron K.M., Ikeda Y., Parker K.L., and Stocco D.M. Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol. Endocrinol. 9 (1995) 1346-1355
11. Clark B.J., Wells J., King S.R., and Stocco D.M. 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 (1994) 28314-28322
12. Constantinescu A., Gordon A.S., and Diamond I. cAMP-dependent protein kinase types I and II differentially regulate cAMP response element-mediated gene expression: implications for neuronal responses to ethanol. J. Biol. Chem. 277 (2002) 18810-18816
13. Constantinescu A., Wu M., Asher O., and Diamond I. cAMP-dependent protein kinase type I regulates ethanol-induced cAMP response element-mediated gene expression via activation of CREB-binding protein and inhibition of MAPK. J. Biol. Chem. 279 (2004) 43321-43329
14. Duan H., and Jefcoate C.R. The predominant cAMP-stimulated 3 × 5 kb StAR mRNA contains specific sequence elements in the extended 3′UTR that confer high basal instability. J. Mol. Endocrinol. 38 (2007) 159-179
15. Dyson M.T., Jones J.K., Kowalewski M.P., Manna P.R., Alonso M., Gottesman M.E., and Stocco D.M. Mitochondrial A-kinase anchoring protein 121 binds type II protein kinase A and enhances steroidogenic acute regulatory protein-mediated steroidogenesis in MA-10 mouse leydig tumor cells. Biol. Reprod. 78 (2008) 267-277
16. Feliciello A., Gottesman M.E., and Avvedimento E.V. The biological functions of A-kinase anchor proteins. J. Mol. Biol. 308 (2001) 99-114
17. Fleury A., Mathieu A.P., Ducharme L., Hales D.B., and LeHoux J.G. Phosphorylation and function of the hamster adrenal steroidogenic acute regulatory protein (StAR). J. Steroid Biochem. Mol. Biol. 91 (2004) 259-271
18. Fong T.H., and Wang S.M. Dissection of the signaling mechanism for capsule detachment of lipid droplets in rat adrenocortical cells. J. Cell. Biochem. 65 (1997) 67-74
19. Gill G.N., and Garren L.D. Role of the receptor in the mechanism of action of adenosine 3′:5′-cyclic monophosphate. Proc. Natl. Acad. Sci. U.S.A. 68 (1971) 786-790
20. Hipkin R.W., and Moger W.H. Type 1 and 2 isoenzymes of cAMP-dependent protein kinase in Leydig cell steroidogenesis. Mol. Cell. Endocrinol. 77 (1991) 91-96
21. Hunzicker-Dunn M., and Jungmann R.A. Rabbit ovarian protein kinases. I. Effect of an ovulatory dose of human chorionic gonadotropin or luteinizing hormone on the subcellular distribution of follicular and luteal protein kinases. Endocrinology 103 (1978) 420-430
22. Hunzicker-Dunn M., and Jungmann R.A. Rabbit ovarian protein kinases. II. Effect of an ovulatory dose of human chorionic gonadotropin or luteinizing hormone on the multiplicity of follicular and luteal protein kinases. Endocrinology 103 (1978) 431-440
23. Ishigaki Y., Li X., Serin G., and Maquat L.E. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106 (2001) 607-617
24. Jo Y., King S.R., Khan S.A., and Stocco D.M. Involvement of protein kinase C and cyclic adenosine 3′,5′-monophosphate-dependent kinase in steroidogenic acute regulatory protein expression and steroid biosynthesis in Leydig cells. Biol. Reprod. 73 (2005) 244-255
25. Kallen C.B., Arakane F., Christenson L.K., Watari H., Devoto L., and Strauss III J.F. Unveiling the mechanism of action and regulation of the steroidogenic acute regulatory protein. Mol. Cell. Endocrinol. 145 (1998) 39-45
26. Katsumata N., Tanae A., Sato N., Horikawa R., and Tanaka M. Adrenal gland. Significance of new StAR gene mutation of S195A-StAR phosphorylation found in congenital adrenal lipoid hyperplasia. Clin. Endocrinol. 48 (2000) 141-143
27. King S.R., and Stocco D.M. ATP and a mitochondrial electrochemical gradient are required for functional activity of the steroidogenic acute regulatory (StAR) protein in isolated mitochondria. Endocr. Res. 22 (1996) 505-514
28. Koroscil T.M., and Gallant S. The phosphorylation of adrenal proteins in response to adrenocorticotropic hormone. J. Biol. Chem. 256 (1981) 6700-6707
29. Kowalewski M.P., Schuler G., Taubert A., Engel E., and Hoffmann B. Expression of cyclooxygenase 1 and 2 in the canine corpus luteum during diestrus. Theriogenology 66 (2006) 1423-1430
30. Kraemer F.B., Shen W.J., Harada K., Patel S., Osuga J., Ishibashi S., and Azhar S. Hormone-sensitive lipase is required for high-density lipoprotein cholesteryl ester-supported adrenal steroidogenesis. Mol. Endocrinol. 18 (2004) 549-557
31. Kraemer F.B., Shen W.J., Patel S., Osuga J., Ishibashi S., and Azhar S. The LDL receptor is not necessary for acute adrenal steroidogenesis in mouse adrenocortical cells. Am. J. Physiol. Endocrinol. Metab. 292 (2007) E408-E412
32. Lee P.C., Radloff D., Schweppe J.S., and Jungmann R.A. Testicular protein kinases. Characterization of multiple forms and ontogeny. J. Biol. Chem. 251 (1976) 914-921
33. Liu J., Li H., and Papadopoulos V. PAP7, a PBR/PKA-RIalpha-associated protein: a new element in the relay of the hormonal induction of steroidogenesis. J. Steroid Biochem. Mol. Biol. 85 (2003) 275-283
34. Liu J., Rone M.B., and Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 281 (2006) 38879-38893
35. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
36. Makarevich A.V., Sirotkin A.V., and Genieser H.G. Action of protein kinase A regulators on secretory activity of porcine granulosa cells in vitro. Anim. Reprod. Sci. 81 (2004) 125-136
37. Manna P.R., Dyson M.T., Eubank D.W., Clark B.J., Lalli E., Sassone-Corsi P., Zeleznik A.J., and Stocco D.M. Regulation of steroidogenesis and the steroidogenic acute regulatory protein by a member of the cAMP response-element binding protein family. Mol. Endocrinol. 16 (2002) 184-199
38. Manna P.R., Eubank D.W., Lalli E., Sassone-Corsi P., and Stocco D.M. Transcriptional regulation of the mouse steroidogenic acute regulatory protein gene by the cAMP response-element binding protein and steroidogenic factor 1. J. Mol. Endocrinol. 30 (2003) 381-397
39. Manna P.R., Eubank D.W., and Stocco D.M. Assessment of the role of activator protein-1 on transcription of the mouse steroidogenic acute regulatory protein gene. Mol. Endocrinol. 18 (2004) 558-573
40. Manna P.R., Huhtaniemi I.T., and Stocco D.M. Detection of hCG responsive expression of the steroidogenic acute regulatory protein in mouse leydig cells. Biol. Proced. Online 6 (2004) 83-93
41. Manna P.R., and Stocco D.M. Crosstalk of CREB and Fos/Jun on a single cis-element: transcriptional repression of the steroidogenic acute regulatory protein gene. J. Mol. Endocrinol. 39 (2007) 261-277
42. Mantovani G., Lania A.G., Bondioni S., Peverelli E., Pedroni C., Ferrero S., Pellegrini C., Vicentini L., Arnaldi G., Bosari S., Beck-Peccoz P., and Spada A. Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Exp. Cell Res. 314 (2008) 123-130
43. Maronde E., Wicht H., Tasken K., Genieser H.G., Dehghani F., Olcese J., and Korf H.W. CREB phosphorylation and melatonin biosynthesis in the rat pineal gland: involvement of cyclic AMP dependent protein kinase type II. J. Pineal. Res. 27 (1999) 170-182
44. Miller W.L. Mechanism of StAR's regulation of mitochondrial cholesterol import. Mol. Cell. Endocrinol. 265-266 (2007) 46-50
45. Miller W.L. StAR search-what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Mol. Endocrinol. 21 (2007) 589-601
46. Miller W.L. Steroidogenic acute regulatory protein (StAR), a novel mitochondrial cholesterol transporter. Biochim. Biophys. Acta 1771 (2007) 663-676
47. Moger W.H. Evidence for compartmentalization of adenosine 3′,5′-monophosphate (cAMP)-dependent protein kinases in rat Leydig cells using site-selective cAMP analogs. Endocrinology 128 (1991) 1414-1418
48. Neher R., Milani A., Solano A.R., and Podesta E.J. Compartmentalization of corticotropin-dependent steroidogenic factors in adrenal cortex: evidence for a post-translational cascade in stimulation of the cholesterol side-chain split. Proc. Natl. Acad. Sci. U.S.A. 79 (1982) 1727-1731
49. Ogreid D., Ekanger R., Suva R.H., Miller J.P., Sturm P., Corbin J.D., and Doskeland S.O. Activation of protein kinase isozymes by cyclic nucleotide analogs used singly or in combination. Principles for optimizing the isozyme specificity of analog combinations. Eur. J. Biochem. 150 (1985) 219-227
50. Pon L.A., Hartigan J.A., and Orme-Johnson N.R. Acute ACTH regulation of adrenal corticosteroid biosynthesis. Rapid accumulation of a phosphoprotein. J. Biol. Chem. 261 (1986) 13309-13316
51. Pon L.A., and Orme-Johnson N.R. Acute stimulation of steroidogenesis in corpus luteum and adrenal cortex by peptide hormones. Rapid induction of a similar protein in both tissues. J. Biol. Chem. 261 (1986) 6594-6599
52. Resko J.A., Norman R.L., Niswender G.D., and Spies H.G. The relationship between progestins and gonadotropins during the late luteal phase of the menstrual cycle in rhesus monkeys. Endocrinology 94 (1974) 128-135
53. Shen W.J., Patel S., Natu V., Hong R., Wang J., Azhar S., and Kraemer F.B. Interaction of hormone-sensitive lipase with steroidogenic acute regulatory protein: facilitation of cholesterol transfer in adrenal. J. Biol. Chem. 278 (2003) 43870-43876
54. Skalhegg B.S., Landmark B.F., Doskeland S.O., Hansson V., Lea T., and Jahnsen T. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effects of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. J. Biol. Chem. 267 (1992) 15707-15714
55. Skalhegg B.S., and Tasken K. Specificity in the cAMP/PKA signaling pathway. Differential expression, regulation, and subcellular localization of subunits of PKA. Front Biosci. 5 (2000) D678-693
56. Stocco D.M., and Chaudhary L.R. Evidence for the functional coupling of cyclic AMP in MA-10 mouse Leydig tumour cells. Cell Signal. 2 (1990) 161-170
57. Stocco D.M., and Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17 (1996) 221-244
58. Stocco D.M., and Sodeman T.C. 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 (1991) 19731-19738
59. Stocco D.M., Wang X., Jo Y., and Manna P.R. Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol. Endocrinol. 19 (2005) 2647-2659
60. Stralfors P., and Belfrage P. Phosphorylation of hormone-sensitive lipase by cyclic AMP-dependent protein kinase. J. Biol. Chem. 258 (1983) 15146-15152
61. Taylor S.S., Buechler J.A., and Yonemoto W. cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu. Rev. Biochem. 59 (1990) 971-1005
62. Wang X.J., Dyson M.T., Jo Y., Eubank D.W., and Stocco D.M. Involvement of 5-lipoxygenase metabolites of arachidonic acid in cyclic AMP-stimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J. Steroid Biochem. Mol. Biol. 85 (2003) 159-166
63. Wang X.J., Dyson M.T., Mondillo C., Patrignani Z., Pignataro O., and Stocco D.M. Interaction between arachidonic acid and cAMP signaling pathways enhances steroidogenesis and StAR gene expression in MA-10 Leydig tumor cells. Mol. Cell. Endocrinol. 188 (2002) 55-63
64. Whitehouse B.J., and Abayasekara D.R. Roles of type I and type II isoenzymes of cyclic AMP-dependent protein kinase in steroidogenesis in rat adrenal cells. J. Mol. Endocrinol. 12 (1994) 195-202
65. Wong W., and Scott J.D. AKAP signalling complexes: focal points in space and time. Nat. Rev. Mol. Cell. Biol. 5 (2004) 959-970
66. Yeaman S.J. Hormone-sensitive lipase-new roles for an old enzyme. Biochem. J. 379 (2004) 11-22
67. Zhao D., Duan H., Kim Y.C., and Jefcoate C.R. Rodent StAR mRNA is substantially regulated by control of mRNA stability through sites in the 3′-untranslated region and through coupling to ongoing transcription. J. Steroid Biochem. Mol. Biol. 96 (2005) 155-173