CAMP stimulation of StAR expression and cholesterol metabolism is modulated by co-expression of labile suppressors of transcription and mRNA turnover

Molecular and Cellular Endocrinology

Volumn 336, Issue 1-2, 2011, Pages 53-62

  Jefcoate, Colin R ^a   Lee, Jinwoo ^a   Cherradi, Nadia ^b   Takemori, Hiroshi ^c   Duan, Haichuan ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b INSERM   (France)

^c NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

Author keywords

Adrenal; CAMP; Cholesterol metabolism; SIK; StAR; TIS11b

Indexed keywords

CHOLESTEROL; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN REGULATED TRANSCRIPTION COACTIVATOR; HISTONE DEACETYLASE 2; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE; PROTEIN TLS11B; SALT INDUCIBLE KINASE; SMALL INTERFERING RNA; STAUROSPORINE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROIDOGENIC FACTOR 1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

3' UNTRANSLATED REGION; ADRENAL CELL; CHOLESTEROL METABOLISM; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; RNA STABILITY;

3' UNTRANSLATED REGIONS; ANIMALS; CHOLESTEROL; CYCLIC AMP; HUMANS; PHOSPHOPROTEINS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 79952070873     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.12.006     Document Type: Review

References (56)

1. Adams D.G., Coffee R.L., Zhang H., Pelech S., Strack S., Wadzinski B.E. Positive regulation of Raf1-MEK1/2-ERK1/2 signaling by protein serine/threonine phosphatase 2A holoenzymes. J. Biol. Chem. 2005, 280:42644-42654.
2. Al-Hakim A.K., Goransson O., Deak M., Toth R., Campbell D.G., Morrice N.A., Prescott A.R., Alessi D.R. 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J. Cell Sci. 2005, 118:5661-5673.
3. Ariyoshi N., Kim Y.C., Artemenko I., Bhattacharyya K.K., 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. 1998, 273:7610-7619.
4. Artemenko I.P., Zhao D., Hales D.B., Hales K.H., Jefcoate C.R. 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. 2001, 276:46583-46596.
5. Asirvatham A.J., Magner W.J., Tomasi T.B. miRNA regulation of cytokine genes. Cytokine 2009, 45:58-69.
6. Bakheet T., Frevel M., Williams B.R., Greer W., Khabar K.S. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res. 2001, 29:246-254.
7. Berdeaux R., Goebel N., Banaszynski L., Takemori H., Wandless T., Shelton G.D., Montminy M. SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes. Nat. Med. 2007, 13:597-603.
8. Bose M., Whittal R.M., Miller W.L., Bose H.S. Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein. J. Biol. Chem. 2008, 283:8837-8845.
9. Chen C.Y., Xu N., Shyu A.B. Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol. Cell. Biol. 2002, 22:7268-7278.
10. Cherradi N., Lejczak C., Desroches-Castan A., Feige J.J. Antagonistic functions of tetradecanoyl phorbol acetate-inducible-sequence 11b and HuR in the hormonal regulation of vascular endothelial growth factor messenger ribonucleic acid stability by adrenocorticotropin. Mol. Endocrinol. 2006, 20:916-930.
11. Chinn A.M., Ciais D., Bailly S., Chambaz E., LaMarre J., Feige J.J. Identification of two novel ACTH-responsive genes encoding manganese-dependent superoxide dismutase (SOD2) and the zinc finger protein TIS11b [tetradecanoyl phorbol acetate (TPA)-inducible sequence 11b]. Mol. Endocrinol. 2002, 16:1417-1427.
12. Ciais D., Cherradi N., Bailly S., Grenier E., Berra E., Pouyssegur J., Lamarre J., Feige J.J. Destabilization of vascular endothelial growth factor mRNA by the zinc-finger protein TIS11b. Oncogene 2004, 23:8673-8680.
13. Clark B.J., Combs R. Angiotensin II and cyclic adenosine 3',5'-monophosphate induce human steroidogenic acute regulatory protein transcription through a common steroidogenic factor-1 element. Endocrinology 1999, 140:4390-4398.
14. Clark B.J., Soo S.C., Caron K.M., Ikeda Y., Parker K.L., Stocco D.M. Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Mol. Endocrinol. 1995, 9:1346-1355.
15. Clem B.F., Hudson E.A., Clark B.J. Cyclic adenosine 3',5'-monophosphate (cAMP) enhances cAMP-responsive element binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory protein gene promoter. Endocrinology 2005, 146:1348-1356.
16. Duan H., Cherradi N., Feige J.J., Jefcoate C. cAMP-dependent posttranscriptional regulation of steroidogenic acute regulatory (StAR) protein by the zinc finger protein ZFP36L1/TIS11b. Mol. Endocrinol. 2009, 23:497-509.
17. Duan H., Jefcoate C.R. The predominant cAMP-stimulated 3×5kb StAR mRNA contains specific sequence elements in the extended 3'UTR that confer high basal instability. J. Mol. Endocrinol. 2007, 38:159-179.
18. Dyson M.T., Jones J.K., Kowalewski M.P., Manna P.R., Alonso M., Gottesman M.E., 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. 2008, 78:267-277.
19. Dyson M.T., Kowalewski M.P., Manna P.R., Stocco D.M. The differential regulation of steroidogenic acute regulatory protein-mediated steroidogenesis by type I and type II PKA in MA-10 cells. Mol. Cell. Endocrinol. 2009, 300:94-103.
20. Fan X.C., Steitz J.A. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:15293-15298.
21. Ginsberg M.D., Feliciello A., Jones J.K., Avvedimento E.V., Gottesman M.E. PKA-dependent binding of mRNA to the mitochondrial AKAP121 protein. J. Mol. Biol. 2003, 327:885-897.
22. Grosset C., Chen C.Y., Xu N., Sonenberg N., Jacquemin-Sablon H., Shyu A.B. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 2000, 103:29-40.
23. Guhaniyogi J., Brewer G. Regulation of mRNA stability in mammalian cells. Gene 2001, 265:11-23.
24. Haidan A., Bornstein S.R., Liu Z., Walsh L.P., Stocco D.M., Ehrhart-Bornstein M. Expression of adrenocortical steroidogenic acute regulatory (StAR) protein is influenced by chromaffin cells. Mol. Cell. Endocrinol. 2000, 165:25-32.
25. Hiroi H., Christenson L.K., Chang L., Sammel M.D., Berger S.L., Strauss J.F. Temporal and spatial changes in transcription factor binding and histone modifications at the steroidogenic acute regulatory protein (StAR) locus associated with StAR transcription. Mol. Endocrinol. 2004, 18:791-806.
26. Hudson B.P., Martinez-Yamout M.A., Dyson H.J., Wright P.E. Recognition of the mRNA AU-rich element by the zinc finger domain of TIS11d. Nat. Struct. Mol. Biol. 2004, 11:257-264.
27. Ivell R., Tillmann G., Wang H., Nicol M., Stewart P.M., Bartlick B., Walther N., Mason J.I., Morley S.D. Acute regulation of the bovine gene for the steroidogenic acute regulatory protein in ovarian theca and adrenocortical cells. J. Mol. Endocrinol. 2000, 24:109-118.
28. Jefcoate C. High-flux mitochondrial cholesterol trafficking, a specialized function of the adrenal cortex. J. Clin. Invest. 2002, 110:881-890.
29. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fritzler M.J., Scheuner D., Kaufman R.J., Golan D.E., Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 2005, 169:871-884.
30. Lemm I., Ross J. Regulation of c-myc mRNA decay by translational pausing in a coding region instability determinant. Mol. Cell. Biol. 2002, 22:3959-3969.
31. Li D., Urs A.N., Allegood J., Leon A., Merrill A.H., Sewer M.B. Cyclic AMP-stimulated interaction between steroidogenic factor 1 and diacylglycerol kinase theta facilitates induction of CYP17. Mol. Cell. Biol. 2007, 27:6669-6685.
32. Lin X., Takemori H., Doi J., Katoh Y., Okamoto M. SIK (salt-inducible kinase): regulation of ACTH-mediated steroidogenic gene expression and nuclear/cytosol redistribution. Endocr. Res. 2000, 26:995-1002.
33. Liu J., Rone M.B., Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 2006, 281:38879-38893.
34. Manna P.R., Dyson M.T., Eubank D.W., Clark B.J., Lalli E., Sassone-Corsi P., Zeleznik A.J., 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. 2002, 16:184-199.
35. Manna P.R., Eubank D.W., Lalli E., Sassone-Corsi P., 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. 2003, 30:381-397.
36. Matsumoto K., Wassarman K.M., Wolffe A.P. Nuclear history of a pre-mRNA determines the translational activity of cytoplasmic mRNA. EMBO J. 1998, 17:2107-2121.
37. Meisner N.C., Hackermuller J., Uhl V., Aszodi A., Jaritz M., Auer M. mRNA openers and closers: modulating AU-rich element-controlled mRNA stability by a molecular switch in mRNA secondary structure. Chembiochem 2004, 5:1432-1447.
38. Myer V.E., Fan X.C., Steitz J.A. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 1997, 16:2130-2139.
39. Noubissi F.K., Elcheva I., Bhatia N., Shakoori A., Ougolkov A., Liu J., Minamoto T., Ross J., Fuchs S.Y., Spiegelman V.S. CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signalling. Nature 2006, 441:898-901.
40. Ogilvie R.L., Abelson M., Hau H.H., Vlasova I., Blackshear P.J., Bohjanen P.R. Tristetraprolin down-regulates IL-2 gene expression through AU-rich element-mediated mRNA decay. J. Immunol. 2005, 174:953-961.
41. Phillips R.S., Ramos S.B., Blackshear P.J. Members of the tristetraprolin family of tandem CCCH zinc finger proteins exhibit CRM1-dependent nucleocytoplasmic shuttling. J. Biol. Chem. 2002, 277:11606-11613.
42. Raineri I., Wegmueller D., Gross B., Certa U., Moroni C. Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res. 2004, 32:1279-1288.
43. Ross J. mRNA stability in mammalian cells. Microbiol. Rev. 1995, 59:423-450.
44. Sarkar B., Lu J.Y., Schneider R.J. Nuclear import and export functions in the different isoforms of the AUF1/heterogeneous nuclear ribonucleoprotein protein family. J. Biol. Chem. 2003, 278:20700-20707.
45. Schmidlin M., Lu M., Leuenberger S.A., Stoecklin G., Mallaun M., Gross B., Gherzi R., Hess D., Hemmings B.A., Moroni C. The ARE-dependent mRNA-destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J. 2004, 23:4760-4769.
46. Screaton R.A., Conkright M.D., Katoh Y., Best J.L., Canettieri G., Jeffries S., Guzman E., Niessen S., Yates J.R., Takemori H., et al. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 2004, 119:61-74.
47. Silverman E., Yivgi-Ohana N., Sher N., Bell M., Eimerl S., Orly J. Transcriptional activation of the steroidogenic acute regulatory protein (StAR) gene: GATA-4 and CCAAT/enhancer-binding protein beta confer synergistic responsiveness in hormone-treated rat granulosa and HEK293 cell models. Mol. Cell. Endocrinol. 2006, 252:92-101.
48. Sjostrom M., Stenstrom K., Eneling K., Zwiller J., Katz A.I., Takemori H., Bertorello A.M. SIK1 is part of a cell sodium-sensing network that regulates active sodium transport through a calcium-dependent process. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:16922-16927.
49. Son G.H., Chung S., Choe H.K., Kim H.D., Baik S.M., Lee H., Lee H.W., Choi S., Sun W., Kim H., et al. Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20970-20975.
50. Stephenson A., Huang G.Y., Nguyen N.T., Reuter S., McBride J.L., Ruiz J.C. snf1lk encodes a protein kinase that may function in cell cycle regulation. Genomics 2004, 83:1105-1115.
51. Stocco D.M. Tracking the role of a star in the sky of the new millennium. Mol. Endocrinol. 2001, 15:1245-1254.
52. Stumpo D.J., Byrd N.A., Phillips R.S., Ghosh S., Maronpot R.R., Castranio T., Meyers E.N., Mishina Y., Blackshear P.J. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the Tristetraprolin family. Mol. Cell. Biol. 2004, 24:6445-6455.
53. Takemori H., Kajimura J., Okamoto M. TORC-SIK cascade regulates CREB activity through the basic leucine zipper domain. FEBS J. 2007, 274:3202-3209.
54. Takemori H., Okamoto M. Regulation of CREB-mediated gene expression by salt inducible kinase. J. Steroid Biochem. Mol. Biol. 2008, 108:287-291.
55. Yang W.H., Heaton J.H., Brevig H., Mukherjee S., Iniguez-Lluhi J.A., Hammer G.D. SUMOylation inhibits SF-1 activity by reducing CDK7-mediated serine 203 phosphorylation. Mol. Cell. Biol. 2009, 29:613-625.
56. Zhao D., Duan H., Kim Y.C., 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. 2005, 96:155-173.