Circadian expression of steroidogenic cytochromes P450 in the mouse adrenal gland - Involvement of cAMP-responsive element modulator in epigenetic regulation of Cyp17a1

FEBS Journal

Volumn 279, Issue 9, 2012, Pages 1584-1593

  Košir, Rok ^a   Zmrzljak, Ursula Prosenc ^a   Bele, Tanja ^a   Acimovic, Jure ^a   Perse, Martina ^a   Majdic, Gregor ^a,b   Prehn, Cornelia ^c   Adamski, Jerzy ^c   Rozman, Damjana ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b UNIVERSITY OF MARIBOR   (Slovenia)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

cAMP responsive element modulator (CREM); circadian; corticosterone; CYP17A1; DNA methylation

Indexed keywords

CORTICOSTEROID; CYTOCHROME P450;

ADRENAL GLAND; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYCLIC AMP RESPONSIVE ELEMENT; CYP11A1 GENE; CYP11B1 GENE; CYP11B2 GENE; CYP17A1 GENE; CYP21A1 GENE; CYP51 GENE; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION; GENE REPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEROIDOGENESIS;

ADRENAL GLANDS; ANIMALS; CIRCADIAN RHYTHM; CORTICOSTERONE; CYCLIC AMP RESPONSE ELEMENT MODULATOR; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MICE; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; STEROID 17-ALPHA-HYDROXYLASE;

MUS;

EID: 84860215808     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08317.x     Document Type: Article

References (37)

1. Coon MJ, (2005) Cytochrome P450: nature's most versatile biological catalyst. Annu Rev Pharmacol Toxicol 45, 1-25. (Pubitemid 40261796)
2. Seliskar M, &, Rozman D, (2007) Mammalian cytochromes P450-importance of tissue specificity. Biochim Biophys Acta 1770, 458-466. (Pubitemid 46136750)
3. Kemppainen RJ, &, Behrend EN, (1997) Adrenal physiology. Vet Clin North Am Small Anim Pract 27, 173-186.
4. Missaghian E, Kempna P, Dick B, Hirsch A, Alikhani-Koupaei R, Jegou B, Mullis PE, Frey BM, &, Fluck CE, (2009) Role of DNA methylation in the tissue-specific expression of the CYP17A1 gene for steroidogenesis in rodents. J Endocrinol 202, 99-109.
5. Oster H, Damerow S, Hut RA, &, Eichele G, (2006) Transcriptional profiling in the adrenal gland reveals circadian regulation of hormone biosynthesis genes and nucleosome assembly genes. J Biol Rhythms 21, 350-361. (Pubitemid 44387427)
6. Oster H, Damerow S, Kiessling S, Jakubcakova V, Abraham D, Tian J, Hoffmann MW, &, Eichele G, (2006) The circadian rhythm of glucocorticoids is regulated by a gating mechanism residing in the adrenal cortical clock. Cell Metab 4, 163-173. (Pubitemid 44138721)
7. Reddy AB, Maywood ES, Karp NA, King VM, Inoue Y, Gonzalez FJ, Lilley KS, Kyriacou CP, &, Hastings MH, (2007) Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45, 1478-1488. (Pubitemid 46918332)
8. Chung S, Son GH, &, Kim K, (2011) Adrenal peripheral oscillator in generating the circadian glucocorticoid rhythm. Ann N Y Acad Sci 1220, 71-81.
9. Green CB, Takahashi JS, &, Bass J, (2008) The meter of metabolism. Cell 134, 728-742.
10. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G, McDearmon E, Laposky A, Losee-Olson S, Easton A, Jensen DR, et al. (2005) Obesity and metabolic syndrome in circadian clock mutant mice. Science 308, 1043-1045. (Pubitemid 40664419)
11. Sewer MB, &, Waterman MR, (2001) Insights into the transcriptional regulation of steroidogenic enzymes and StAR. Rev Endocr Metab Disord 2, 269-274. (Pubitemid 33640576)
12. Foulkes NS, Whitmore D, &, Sassone-Corsi P, (1997) Rhythmic transcription: the molecular basis of circadian melatonin synthesis. Biol Cell 89, 487-494. (Pubitemid 28209696)
13. Acimovic J, Fink M, Pompon D, Bjorkhem I, Hirayama J, Sassone-Corsi P, Golicnik M, &, Rozman D, (2008) CREM modulates the circadian expression of CYP51, HMGCR and cholesterogenesis in the liver. Biochem Biophys Res Commun 376, 206-210.
14. Borjigin J, Wang MM, &, Snyder SH, (1995) Diurnal variation in mRNA encoding serotonin N-acetyltransferase in pineal gland. Nature 378, 783-785. (Pubitemid 26004410)
15. Lopez-Serra L, Ballestar E, Ropero S, Setien F, Billard LM, Fraga MF, Lopez-Nieva P, Alaminos M, Guerrero D, Dante R, et al. (2008) Unmasking of epigenetically silenced candidate tumor suppressor genes by removal of methyl-CpG-binding domain proteins. Oncogene 27, 3556-3566. (Pubitemid 351793801)
16. Son GH, Chung S, Choe HK, Kim HD, Baik SM, Lee H, Lee HW, Choi S, Sun W, Kim H, et al. (2008) Adrenal peripheral clock controls the autonomous circadian rhythm of glucocorticoid by causing rhythmic steroid production. Proc Natl Acad Sci USA 105, 20970-20975.
17. Carnes M, Kalin NH, Lent SJ, Barksdale CM, &, Brownfield MS, (1988) Pulsatile ACTH secretion: variation with time of day and relationship to cortisol. Peptides 9, 325-331. (Pubitemid 19260239)
18. Sewer MB, Dammer EB, &, Jagarlapudi S, (2007) Transcriptional regulation of adrenocortical steroidogenic gene expression. Drug Metab Rev 39, 371-388. (Pubitemid 47364558)
19. Ishida A, Mutoh T, Ueyama T, Bando H, Masubuchi S, Nakahara D, Tsujimoto G, &, Okamura H, (2005) Light activates the adrenal gland: timing of gene expression and glucocorticoid release. Cell Metab 2, 297-307.
20. Le Goascogne C, Sananes N, Gouezou M, Takemori S, Kominami S, Baulieu EE, &, Robel P, (1991) Immunoreactive cytochrome P-450(17 alpha) in rat and guinea-pig gonads, adrenal glands and brain. J Reprod Fertil 93, 609-622.
21. Nason TF, Han XG, &, Hall PF, (1992) Cyclic AMP regulates expression of the rat gene for steroid 17 alpha-hydroxylase/C17-20 lyase P-450 (CYP17) in rat Leydig cells. Biochim Biophys Acta 1171, 73-80.
22. Rodriguez H, Hum DW, Staels B, &, Miller WL, (1997) Transcription of the human genes for cytochrome P450scc and P450c17 is regulated differently in human adrenal NCI-H295 cells than in mouse adrenal Y1 cells. J Clin Endocrinol Metab 82, 365-371. (Pubitemid 27068593)
23. Sewer MB, Li D, Dammer EB, Jagarlapudi S, &, Lucki N, (2008) Multiple signaling pathways coordinate CYP17 gene expression in the human adrenal cortex. Acta Chim Slov 55, 53-57.
24. de Groot RP, &, Sassone-Corsi P, (1993) Hormonal control of gene expression: multiplicity and versatility of cyclic adenosine 3',5'-monophosphate-responsive nuclear regulators. Mol Endocrinol 7, 145-153. (Pubitemid 23066856)
25. Blocher S, Behr R, Weinbauer GF, Bergmann M, &, Steger K, (2003) Expression of CREM isoforms in human and equine testis with normal and impaired spermatogenesis. Andrologia 35, 3-4.
26. Foulkes NS, Mellstrom B, Benusiglio E, &, Sassone-Corsi P, (1992) Developmental switch of CREM function during spermatogenesis: from antagonist to activator. Nature 355, 80-84.
27. Desdouets C, Matesic G, Molina CA, Foulkes NS, Sassone-Corsi P, Brechot C, &, Sobczak-Thepot J, (1995) Cell cycle regulation of cyclin A gene expression by the cyclic AMP-responsive transcription factors CREB and CREM. Mol Cell Biol 15, 3301-3309.
28. Borlikova G, &, Endo S, (2009) Inducible cAMP early repressor (ICER) and brain functions. Mol Neurobiol 40, 73-86.
29. Molina CA, Foulkes NS, Lalli E, &, Sassone-Corsi P, (1993) Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell 75, 875-886. (Pubitemid 24014545)
30. Malisch JL, Breuner CW, Gomes FR, Chappell MA, &, Garland T Jr, (2008) Circadian pattern of total and free corticosterone concentrations, corticosteroid-binding globulin, and physical activity in mice selectively bred for high voluntary wheel-running behavior. Gen Comp Endocrinol 156, 210-217.
31. Wang YH, Tee MK, &, Miller WL, (2010) Human cytochrome p450c17: single step purification and phosphorylation of serine 258 by protein kinase a. Endocrinology 151, 1677-1684.
32. Kempna P, Hirsch A, Hofer G, Mullis PE, &, Fluck CE, (2010) Impact of differential P450c17 phosphorylation by cAMP stimulation and by starvation conditions on enzyme activities and androgen production in NCI-H295R cells. Endocrinology 151, 3686-3696.
33. Dammer EB, &, Sewer MB, (2008) Phosphorylation of CtBP1 by cAMP-dependent protein kinase modulates induction of CYP17 by stimulating partnering of CtBP1 and 2. J Biol Chem 283, 6925-6934.
34. Kosir R, Acimovic J, Golicnik M, Perse M, Majdic G, Fink M, &, Rozman D, (2010) Determination of reference genes for circadian studies in different tissues and mouse strains. BMC Mol Biol 11, 60.
35. Fink M, Acimovic J, Rezen T, Tansek N, &, Rozman D, (2005) Cholesterogenic lanosterol 14alpha-demethylase (CYP51) is an immediate early response gene. Endocrinology 146, 5321-5331. (Pubitemid 41653045)
36. Sambrook J, Fritsch EF, &, Maniatis TM, (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Cornelia P, Ferdinand H, &, Jerzy A, (2010) Quantification of steroids in human and mouse plasma using online solid phase extraction coupled to liquid chromatography tandem mass spectrometry. Nature Protocols, Protocol Exchange, doi:, on-line 16. Feb 2010.