Resveratrol stimulates cortisol biosynthesis by activating SIRT-dependent deacetylation of P450scc

Endocrinology

Volumn 153, Issue 7, 2012, Pages 3258-3268

  Li, Donghui ^a   Dammer, Eric B ^b   Sewer, Marion B ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450; CYTOCHROME P450 11BETA; HYDROCORTISONE; HYDROLASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; PREGNENOLONE; PYRIDINE NUCLEOTIDE; RESVERATROL; SIRTUIN; SIRTUIN 3; SIRTUIN 5; SIRTUIN DEACETYLASE; UNCLASSIFIED DRUG;

ACETYLATION; ADRENAL CORTEX CELL; ARTICLE; CONTROLLED STUDY; DEACETYLATION; DRUG EFFECT; DRUG HALF LIFE; ENZYME ACTIVITY; GENE OVEREXPRESSION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIOXIDANTS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROCORTISONE; LYSINE; MITOCHONDRIA; MUTAGENESIS; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA INTERFERENCE; SIRTUIN 1; SIRTUIN 3; SIRTUINS; STILBENES;

EID: 84862741341     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-2088     Document Type: Article

References (87)

1. Dammer EB, Sewer MB 2008 Phosphorylation of CtBP1 by PKA modulates induction of CYP17 by stimulating partnering of CtBP1 and 2. J Biol Chem 283:6925-6934
2. McKerns KW 1964 Mechanism of action of adrenocorticotropin hormone through activation of glucose-6-phosphate dehydrogenase. Biochim Biophys Acta 90:357-371
3. Criss WE, McKerns KW 1968 Activation of cow adrenal glucose-6-phosphate dehydrogenase by adrenocorticotropin. Biochemistry 7:2364-2368
4. Yang T, Sauve AA 2006 NAD metabolism and sirtuins: metabolic regulation of protein deacetylation in stress and toxicity. AAPS J 8:E632-E643 (Pubitemid 44644162)
5. Yang T, Fu M, Pestell R, Sauve AA 2006 SIRT1 and endocrine signaling. Trends Endocrinol Metab 17:186-191 (Pubitemid 43974972)
6. Michan S, Sinclair D 2007 Sirtuins in mammals: insights into their biological function. Biochem J 404:1-13 (Pubitemid 46788079)
7. Denu JM 2005 The Sir 2 family of protein deacetylases. Curr Opin Chem Biol 9:431-440
8. Buck SW, Gallo CM, Smith JS 2004 Diversity in the Sir2 family of protein deacetylases. J Leukoc Biol 75:939-950 (Pubitemid 38720634)
9. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W 2005 Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 24:1021-1032 (Pubitemid 40470150)
10. van der Horst A, Tertoolen LG, de Vries-Smits LM, Frye RA, Medema RH, Burgering BM 2004 FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem 279:28873-28879 (Pubitemid 38915754)
11. Kobayashi Y, Furukawa-Hibi Y, Chen C, Horio Y, Isobe K, Ikeda K, Motoyama N 2005 SIRT1 is critical regulator of FOXO-mediated transcription in response to oxidative stress. Int J Mol Med 16:237-243
12. Giannakou ME, Partridge L 2004 The interaction between FOXO and SIRT1: tipping the balance towards survival. Trends Cell Biol 14:408-412 (Pubitemid 39092697)
13. Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, Tran H, Ross SE, Mostoslavsky R, Cohen HY, Hu LS, Cheng HL, Jedrychowski MP, Gygi SP, Sinclair DA, Alt FW, Greenberg ME 2004 Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303:2011-2015 (Pubitemid 38393275)
14. Anastasiou D, Krek W 2006 SIRT1: linking adaptive cellular responses to aging-associated changes in organismal physiology. Physiology (Bethesda) 21:404-410 (Pubitemid 44879249)
15. Ulrich S, Loitsch SM, Rau O, von Knethen A, Brüne B, Schubert-Zsilavecz M, Stein JM 2006 Peroxisome proliferator-activated receptor gamma as a molecular target of resveratrol-induced modulation of polyamine metabolism. Cancer Res 66:7348-7354 (Pubitemid 44197718)
16. Senawong T, Peterson VJ, Avram D, Shepherd DM, Frye RA, Minucci S, Leid M 2003 Involvement of the histone deacetylase SIRT1 in chicken ovalbumin upstream promoter transcription factor (COUP-TF)-interacting protein 2-mediated transcriptional repression. J Biol Chem 278:43041-43050 (Pubitemid 37345919)
17. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW, Guarente L 2004 Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-γ. Nature 429:3771-3776
18. Fu M, Liu M, Sauve AA, Jiao X, Zhang X, Wu X, Powell MJ, Yang T, Gu W, Avantaggiati ML, Pattabiraman N, Pestell TG, Wang F, Quong AA, Wang C, Pestell RG 2006 Hormonal control of androgen receptor function through SIRT1. Mol Cell Biol 26:8122-8135 (Pubitemid 44631010)
19. Bäckesjö CM, Li Y, Lindgren U, Haldosén LA 2006 Activation of Sirt1 decreases adipocyte formation during osteoblast differentiation of mesenchymal stem cells. J Bone Miner Res 21:993-1002
20. Huang JY, Hirschey MD, Shimazu T, Ho L, Verdin E 2010 Mitochondrial sirtuins. Biochimica Biophys Acta 1804:1645-1651
21. Hirschey MD, Shimazu T, Goetzman E, Jing E, Schwer B, Lombard DB, Grueter CA, Harris C, Biddinger S, Ilkayeva OR, Stevens RD, Li Y, Saha AK, Ruderman NB, Bain JR, Newgard CB, Farese Jr RV, Alt FW, Kahn CR, Verdin E 2010 SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464:121-125
22. Verdin E, Hirschey MD, Finley LW, Haigis MC 2010 Sirtuin regulation of mitochondria: energy production, apoptosis, and signaling. Trends Biochem Sci 35:669-775
23. Bell EL, Emerling BM, Ricoult SJ, Guarente L 2011 SirT3 suppresses hypoxia inducible factor 1α and tumor growth by inhibiting mitochondrial ROS production. Oncogene 30:2986-2996
24. Finley LW, Carracedo A, Lee J, Souza A, Egia A, Zhang J, Teruya-Feldstein J, Moreira PI, Cardoso SM, Clish CB, Pandolfi PP, Haigis MC 2011 SIRT3 opposes reprogramming of cancer cell metabolism through HIFalpha destabilization. Cancer Cell 19:416-428
25. Qiu X, Brown K, Hirschey MD, Verdin E, Chen D 2010 Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 12:662-667
26. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H, Kim HS, Flynn CR, Hill S, Hayes McDonald W, Olivier AK, Spitz DR, Gius D 2010 Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 40:893-904
27. Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E 2006 Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci USA 103:10224-10229 (Pubitemid 44051148)
28. Hallows WC, Lee S, Denu JM 2006 Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103:10230-10235 (Pubitemid 44051149)
29. Cimen H, Han MJ, Yang Y, Tong Q, Koc H, Koc EC 2010 Regulation of succinate dehydrogenase activity by SIRT3 in mammalian mitochondria. Biochemistry 49:304-311
30. Shimazu T, Hirschey MD, Hua L, Dittenhafer-Reed KE, Schwer B, Lombard DB, Li Y, Bunkenborg J, Alt FW, Denu JM, Jacobson MP, Verdin E 2010 SIRT3 deacetylates mitochondrial 3-hydroxy-3-methylglutaryl CoA synthase 2 and regulates ketone body production. Cell Metab 12:654-661
31. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, Valenzuela DM, Yancopoulos GD, Karow M, Blander G, Wolberger C, Prolla TA, Weindruch R, Alt FW, Guarente L 2006 SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic β-cells. Cell 126:941-954 (Pubitemid 44321935)
32. Nakagawa T, Lomb DJ, Haigis MC, Guarente L 2009 SIRT5 deacetylates carbamoyl phosphate synthetase 1 and regulates the urea cycle. Cell 137:560-570
33. Smith CL 2008 A shifting paradigm: histone deacetylases and transcriptional activation. Bioessays 30:15-24
34. Sadoul K, Boyault C, Pabion M, Khochbin S 2008 Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie (Paris) 90:306-312 (Pubitemid 351172566)
35. Glozak MA, Sengupta N, Zhang X, Seto E 2005 Acetylation and deacetylation of non-histone proteins. Gene 363:15-23 (Pubitemid 41691888)
36. Faus H, Haendler B 2006 Post-translational modifications of steroid receptors. Biomed Pharmacother 60:520-528
37. Batta K, Das C, Gadad S, Shandilya J, Kundu TK 2007 Reversible acetylation of non histone proteins: role in cellular function and disease. Subcell Biochem 41:193-212
38. Nagy Z, Tora L 2007 Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26:5341-5357 (Pubitemid 47255920)
39. Ito T 2007 Role of histone modification in chromatin dynamics. J Biochem 141:609-614 (Pubitemid 47014007)
40. Sablin EP, Blind RD, Krylova IN, Ingraham JG, Cai F, Williams JD, Fletterick RJ, Ingraham HA 2009 Structure of SF-1 bound by different phospholipids: evidence for regulatory ligands. Mol Endocrinol 23:25-34
41. Rainey WE, Bird IM, Mason JI 1994 The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol Cell Endocrinol 100:45-50 (Pubitemid 24109525)
42. Staels B, Hum DW, Miller WL 1993 Regulation of steroidogenesis in NCI-H295 cells: a cellular model of the human fetal adrenal. Mol Endocrinol 7:423-433 (Pubitemid 23104530)
43. Huang MC, Miller WL 2001 Creation and activity of COS-1 cells stably expressing the F2 fusion of the human cholesterol side-chain cleavage enzyme system. Endocrinology 142:2569-2576 (Pubitemid 32475761)
44. Harikrishna JA, Black SM, Szklarz GD, Miller WL 1993 Construction and function of fusion enzymes of the human cytochrome P450scc system. DNA Cell Biol 12:371-379 (Pubitemid 23183515)
45. Nazarov PA, Drutsa VL, Miller WL, Shkumatov VM, Luzikov VN, Novikova LA 2003 Formation and functioning of fused cholesterol side-chain cleavage enzymes. DNA Cell Biol 22:243-252 (Pubitemid 36667852)
46. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, Zipkin RE, Chung P, Kisielewski A, Zhang LL, Scherer B, Sinclair DA 2003 Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425:191-196 (Pubitemid 37150899)
47. Mukherjee S, Lekli I, Gurusamy N, Bertelli AA, Das DK 2009 Expression of the longevity proteins by both red and white wines and their chemoprotective components, resveratrol, tyrosol, and hydroxytyrosol. Free Radic Biol Med 46:573-578
48. Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, Yang Y, Chen Y, Hirschey MD, Bronson RT, Haigis M, Guarente LP, Farese Jr RV, Weissman S, Verdin E, Schwer B 2007 Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27:8807-8814
49. Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y 2006 Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23:607-618 (Pubitemid 44205490)
50. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I 2005 Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol Biol Cell 16:4623-4635 (Pubitemid 41416446)
51. North BJ, Verdin E 2007 Interphase nucleo-cytoplasmic shuttling and localization of SIRT2 during mitosis. PLoS ONE 2:e784
52. +-dependent histone deacetylase that translocates to the mitochondria upon cellular stress. Genes Dev 21:920-928
53. Nakamura Y, Ogura M, Tanaka D, Inagaki N 2008 Localization of mouse mitochondrial SIRT proteins: shift of SIRT3 to nucleus by co-expression with SIRT5. Biochem Biophys Res Commun 366:174-179 (Pubitemid 50010675)
54. Cooper HM, Spelbrink JN 2008 The human SIRT3 protein deacetylase is exclusively mitochondrial. Biochem J 411:279-285 (Pubitemid 351580180)
55. Boggaram V, Zuber MX, Waterman MR 1984 Turnover of newly synthesized cytochromes P-450scc and P-450 11b and adrenodoxin in bovine adrenocortical cells in monolayer culture: effect of adrenocorticotropin. Arch Biochem Biophys 231:518-523 (Pubitemid 14120242)
56. Yano JK, Wester MR, Schoch GA, Griffin KJ, Stout CD, Johnson EF 2004 The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05-A resolution. J Biol Chem 279:38091-38094 (Pubitemid 39295952)
57. Novikova LA, Nazarov PA, Saveliev AS, Drutsa VL, Sergeev VN, Miller WL, Luzikov VN 2000 Interaction of catalytic domains in cytochrome P450scc-adrenodoxin reductase-adrenodoxin fusion protein imported into yeast mitochondria. Biochemistry (Mosc) 65:1362-1366 (Pubitemid 33658046)
58. Knights CD, Catania J, Di Giovanni S, Muratoglu S, Perez R, Swartzbeck A, Quong AA, Zhang X, Beerman T, Pestell RG, Avantaggiati ML 2006 Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J Cell Biol 173:533-544 (Pubitemid 43765200)
59. Kohler S, Cirillo LA 2010 Stable chromatin binding prevents FoxA acetylation, preserving FoxA chromatin remodeling. J Biol Chem 285:464-472
60. Ren Q, Gorovsky MA 2001 Histone H2A.Z acetylation modulates an essential charge patch. Mol Cell 7:1329-1335 (Pubitemid 32607365)
61. Wang X, Hayes JJ 2008 Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol Cell Biol 28:227-236
62. Gertz M, Steegborn C 2010 Function and regulation of the mitochondrial sirtuin isoform Sirt5 in mammalia. Biochim Biophys Acta 1804:1658-1665
63. Pacholec M, Bleasdale JE, Chrunyk B, Cunningham D, Flynn D, Garofalo RS, Griffith D, Griffor M, Loulakis P, Pabst B, Qiu X, Stockman B, Thanabal V, Varghese A, Ward J, Withka J, Ahn K 2010 SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 285:8340-8351
64. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S, Xiong Y 2011 Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 12:534-541
65. Hafner AV, Dai J, Gomes AP, Xiao CY, Palmeira CM, Rosenzweig A, Sinclair DA 2010 Regulation of the mPTP by SIRT3-mediated deacetylation of CypD at lysine 166 suppresses age-related cardiac hypertrophy. Aging 2:914-923
66. Hallows WC, Yu W, Smith BC, Devries MK, Devires MK, Ellinger JJ, Someya S, Shortreed MR, Prolla T, Markley JL, Smith LM, Zhao S, Guan KL, Denu JM 2011 Sirt3 promotes the urea cycle and fatty acid oxidation during dietary restriction. Mol Cell 41:139-149
67. Koyama T, Kume S, Koya D, Araki S, Isshiki K, Chin-Kanasaki M, Sugimoto T, Haneda M, Sugaya T, Kashiwagi A, Maegawa H, Uzu T 2011 SIRT3 attenuates palmitate-induced ROS production and inflammation in proximal tubular cells. Free Radic Biol Med 51:1258-1267
68. Dali-Youcef N, Lagouge M, Froelich S, Koehl C, Schoonjans K, Auwerx J 2007 Sirtuins: the 'magnificent seven', function, metabolism and longevity. Ann Med 39:335-345
69. Guarente L 2007 Sirtuins in aging and disease. Cold Spring Harb Symp Quant Biol 72:483-488
70. Milne JC, Denu JM 2008 The sirtuin family: therapeutic targets to treat diseases of aging. Curr Opin Chem Biol 12:11-17
71. Inoue T, Hiratsuka M, Osaki M, Oshimura M 2007 The molecular biology of mammalian SIRT proteins: SIRT2 in cell cycle regulation. Cell Cycle 6:1011-1018 (Pubitemid 46708571)
72. Schwer B, Verdin E 2008 Conserved metabolic regulatory functions of sirtuins. Cell Metab 7:104-112 (Pubitemid 351168554)
73. Hirschey MD, Shimazu T, Jing E, Grueter CA, Collins AM, Aouizerat B, Stančáková A, Goetzman E, Lam MM, Schwer B, Stevens RD, Muehlbauer MJ, Kakar S, Bass NM, Kuusisto J, Laakso M, Alt FW, Newgard CB, Farese Jr RV, Kahn CR, Verdin E 2011 SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol Cell 44:177-190
74. Mast N, Annalora AJ, Lodowski DT, Palczewski K, Stout CD, Pikuleva IA 2011 Structural basis for three-step sequential catalysis by the cholesterol side chain cleavage enzyme CYP11A1. J Biol Chem 286:5607-5613
75. Wu SL, Pan CE, Yu L, Meng KW 2005 Immunosuppression by combined use of cyclosporine and resveratrol in a rat liver transplantation model. Transplant Proc 37:2354-2359 (Pubitemid 40956448)
76. Sharma S, Chopra K, Kulkarni SK, Agrewala JN 2007 Resveratrol and curcumin suppress immune response through CD28/CTLA-4 and CD80 co-stimulatory pathway. Clin Exp Immunol 147:155-163 (Pubitemid 44915567)
77. Hsu JY, Feldman D, McNeal JE, Peehl DM 2001 Reduced 1alpha-hydroxylase activity in human prostate cancer cells correlates with decreased susceptibility to 25-hydroxyvitamin D3-induced growth inhibition. Cancer Res 61:2852-2856 (Pubitemid 32691924)
78. Chen TC 2008 25-Hydroxyvitamin D-1 α-hydroxylase (CYP27B1) is a new class of tumor suppressor in the prostate. Anticancer Res 28:2015-2017
79. Barreto AM, Schwartz GG, Woodruff R, Cramer SD 2000 25-Hydroxyvitamin D3, the prohormone of 1,25-dihydroxyvitamin D3, inhibits the proliferation of primary prostatic epithelial cells. Cancer Epidemiol Biomarkers Prev 9:265-270 (Pubitemid 30165438)
80. Schwartz GG, Eads D, Rao A, Cramer SD, Willingham MC, Chen TC, Jamieson DP, Wang L, Burnstein KL, Holick MF, Koumenis C 2004 Pancreatic cancer cells express 25-hydroxyvitamin D-1 α-hydroxylase and their proliferation is inhibited by the prohormone 25-hydroxyvitamin D3. Carcinogenesis 25:1015-1026 (Pubitemid 38898637)
81. Schlachterman A, Valle F, Wall KM, Azios NG, Castillo L, Morell L, Washington AV, Cubano LA, Dharmawardhane SF 2008 Combined resveratrol, quercetin, and catechin treatment reduces breast tumor growth in a nude mouse model. Transl Oncol 1:19-27
82. Zahid M, Gaikwad NW, Ali MF, Lu F, Saeed M, Yang L, Rogan EG, Cavalieri EL 2008 Prevention of estrogen-DNA adduct formation in MCF-10F cells by resveratrol. Free Radic Biol Med 45:136-145
83. Tang FY, Su YC, Chen NC, Hsieh HS, Chen KS 2008 Resveratrol inhibits migration and invasion of human breast-cancer cells. Mol Nutr Food Res 52:683-691
84. Delmas D, Lançon A, Colin D, Jannin B, Latruffe N 2006 Resveratrol as a chemopreventive agent: a promising molecule for fighting cancer. Curr Drug Targets 7:423-442 (Pubitemid 43744833)
85. Lin HY, Sun M, Tang HY, Simone TM, Wu YH, Grandis JR, Cao HJ, Davis PJ, Davis FB 2008 Resveratrol causes COX-2- and p53-dependent apoptosis in head and neck squamous cell cancer cells. J Cell Biochem 104:2131-2142
86. Athar M, Back JH, Tang X, Kim KH, Kopelovich L, Bickers DR, Kim AL 2007 Resveratrol: a review of preclinical studies for human cancer prevention. Toxicol Appl Pharmacol 224:274-283 (Pubitemid 47575677)
87. Charvet C, Liao WL, Heo GY, Laird J, Salomon RG, Turko IV, Pikuleva IA 2011 Isolevuglandins and mitochondrial enzymes in the retina mass spectrometry detection of post-translational modification of sterol-metabolizing CYP27A1. J Biol Chem 286:20413-20422