Inheritable stimulatory effects of caffeine on steroidogenic acute regulatory protein expression and cortisol production in human adrenocortical cells

Chemico-Biological Interactions

Volumn 195, Issue 1, 2012, Pages 68-75

  Ping, Jie ^a,b,c   Lei, You Ying ^a   Liu, Lian ^a   Wang, Ting Ting ^a,b   Feng, Ying Hong ^b   Wang, Hui ^a,c  

^a WUHAN UNIVERSITY   (China)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c WUHAN UNIVERSITY   (China)

Author keywords

Caffeine; Cortisol; DNA methylation; Steroidogenesis; Steroidogenic acute regulatory protein

Indexed keywords

BISULFITE; CAFFEINE; GENOMIC DNA; HYDROCORTISONE; MESSENGER RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ADRENAL CORTEX CELL; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; HERITABILITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; POLYMERASE CHAIN REACTION; PROMOTER REGION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; STEROIDOGENESIS;

ADRENAL CORTEX; CAFFEINE; CELL LINE; CENTRAL NERVOUS SYSTEM STIMULANTS; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; HYDROCORTISONE; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER;

EID: 82455219042     PISSN: 00092797     EISSN: 18727786     Source Type: Journal    
DOI: 10.1016/j.cbi.2011.11.001     Document Type: Article

References (56)

1. J.J. Barone, and H.R. Roberts Caffeine consumption Food Chem. Toxicol. 34 1996 119 129 (Pubitemid 26057854)
2. R. Dhingra, L. Sullivan, P.F. Jacques, T.J. Wang, C.S. Fox, J.B. Meigs, R.B. D'Agostino, J.M. Gaziano, and R.S. Vasan Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community Circulation 116 2007 480 488 (Pubitemid 47450256)
3. A. Hino, H. Adachi, M. Enomoto, K. Furuki, Y. Shigetoh, M. Ohtsuka, S. Kumagae, Y. Hirai, A. Jalaldin, A. Satoh, and T. Imaizumi Habitual coffee but not green tea consumption is inversely associated with metabolic syndrome: an epidemiological study in a general Japanese population Diabetes Res. Clin. Pract. 76 2007 383 389 (Pubitemid 46482724)
4. J. James, P. Thomas, D. Cavan, and D. Kerr Preventing childhood obesity by reducing consumption of carbonated drinks: cluster randomised controlled trial BMJ 328 2004 1237
5. P. Chanson, and S. Salenave Metabolic syndrome in Cushing's syndrome Neuroendocrinology 92 2010 96 101
6. L.L. Gathercole, and P.M. Stewart Targeting the pre-receptor metabolism of cortisol as a novel therapy in obesity and diabetes J. Steroid Biochem. Mol. Biol. 122 2010 21 27
7. A. Gavrieli, M. Yannakoulia, E. Fragopoulou, D. Margaritopoulos, J.P. Chamberland, P. Kaisari, S.A. Kavouras, and C.S. Mantzoros Caffeinated coffee does not acutely affect energy intake, appetite, or inflammation but prevents serum cortisol concentrations from falling in healthy men J. Nutr. 141 2011 703 707
8. A.S. Lin, T.W. Uhde, S.O. Slate, and U.D. McCann Effects of intravenous caffeine administered to healthy males during sleep Depress. Anxiety 5 1997 21 28 (Pubitemid 28106009)
9. L.F. Pettenuzzo, C. Noschang, E. von Pozzer Toigo, A. Fachin, D. Vendite, and C. Dalmaz Effects of chronic administration of caffeine and stress on feeding behavior of rats Physiol. Behav. 95 2008 295 301
10. A.H. Marques, M.N. Silverman, and E.M. Sternberg Glucocorticoid dysregulations and their clinical correlates. From receptors to therapeutics Ann. N. Y. Acad. Sci. 1179 2009 1 18
11. H.S. Bose, V.R. Lingappa, and W.L. Miller Rapid regulation of steroidogenesis by mitochondrial protein import Nature 417 2002 87 91 (Pubitemid 34498821)
12. P.R. Manna, and D.M. Stocco Regulation of the steroidogenic acute regulatory protein expression: functional and physiological consequences Curr. Drug. Targets. Immune. Endocr. Metabol. Disord. 5 2005 93 108 (Pubitemid 40394307)
13. P.R. Manna, M.T. Dyson, and D.M. Stocco Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives Mol. Hum. Reprod. 15 2009 321 333
14. H.S. Bose, T. Sugawara, J.F. Strauss III, and W.L. Miller The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. International Congenital Lipoid Adrenal Hyperplasia Consortium N. Engl. J. Med. 335 1996 1870 1878 (Pubitemid 26419194)
15. H.S. Bose, R.M. Whittal, Y. Ran, M. Bose, B.Y. Baker, and W.L. Miller StAR-like activity and molten globule behavior of StARD6, A male germ-line protein Biochemistry 47 2008 2277 2288 (Pubitemid 351304534)
16. M. Chen, T. Wang, Z.X. Liao, X.L. Pan, Y.H. Feng, and Y.H. Wang Adrenal-mediated cortisol disturbance in nicotine-induced rat intrauterine growth retardation Exp. Toxicol. Pathol. 3-4 2007 245 251 (Pubitemid 350030442)
17. W.L. Miller StAR search - what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import Mol. Endocrinol. 21 2007 589 601
18. E. Silverman, N. Yivgi-Ohana, N. Sher, M. Bell, S. Eimerl, and J. Orly 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. 252 2006 92 101
19. M. Kraugerud, K.E. Zimmer, E. Dahl, V. Berg, I. Olsaker, W. Farstad, E. Ropstad, and S. Verhaegen Three structurally different polychlorinated biphenyl congeners (Pcb 118, 153, and 126) affect hormone production and gene expression in the human H295R in vitro model J. Toxicol. Environ. Health. A 73 2010 1122 1132
20. W. Li, A.K. Pandey, X. Yin, J.J. Chen, D.M. Stocco, P. Grammas, and X. Wang Effects of apigenin on steroidogenesis and steroidogenic acute regulatory gene expression in mouse Leydig cells J. Nutr. Biochem. 22 2011 212 218
21. M. Ramanjaneya, A.C. Conner, J.E. Brown, J. Chen, J.E. Digby, T.M. Barber, H. Lehnert, and H.S. Randeva Adiponectin (15-36) stimulates steroidogenic acute regulatory (StAR) protein expression and cortisol production in human adrenocortical cells: role of AMPK and MAPK kinase pathways Biochim. Biophys. Acta 1813 2011 802 809
22. I.V. Tkachenko, T. Jääskeläinen, J. Jää skeläinen, J.J. Palvimo, and R. Voutilainen Interleukins 1α and 1β as regulators of steroidogenesis in human NCI-H295R adrenocortical cells Steroids 2011 (Epub ahead of print)
23. G. Klein Epigenetics: surveillance team against cancer Nature 434 2005 150 (Pubitemid 40388033)
24. P.M. Das, and R. Singal DNA methylation and cancer J. Clin. Oncol. 22 2004 4632 4642 (Pubitemid 41185132)
25. J. Liu, X.D. Li, and A. Vaheri R.Voutilainen, DNA methylation affects cell proliferation, cortisol secretion and steroidogenic gene expression in human adrenocortical NCI-H295R cells J. Mol. Endocrinol. 33 2004 651 662 (Pubitemid 40057560)
26. D.J. Kwon, C.K. Park, B.K. Yang, and H.T. Cheong Control of nuclear remodelling and subsequent in vitro development and methylation status of porcine nuclear transfer embryos Reproduction 135 2008 649 656 (Pubitemid 351676449)
27. A. Dardis, and W.L. Miller Dexamethasone does not exert direct intracellular feedback on steroidogenesis in human adrenal NCI-H295A cells J. Endocrinol. 179 2003 131 142 (Pubitemid 37321575)
28. A. Lorente, W. Mueller, E. Urdangarin, P. Lazcoz, A. von Deimling, and J.S. Castresana Detection of methylation in promoter sequences by melting curve analysis-based semiquantitative real time PCR BMC Cancer 8 2008 61
29. J.G. Herman, J.R. Graff, S. Myohanen, B.D. Nelkin, and S.B. Baylin Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands Proc. Natl Acad. Sci. USA 93 1996 9821 9826 (Pubitemid 26296693)
30. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science 308 2005 1466 1469 (Pubitemid 40791300)
31. T.B. Franklin, and I.M. Mansuy Epigenetic inheritance in mammals: evidence for the impact of adverse environmental effects Neurobiol. Dis. 39 2010 61 65
32. R.M. Sapolsky, L.M. Romero, and A.U. Munck How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions Endocr. Rev. 21 2000 55 89 (Pubitemid 32266068)
33. H. Rodriguez, D.W. Hum, B. Staels, and W.L. Miller 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 1997 365 371 (Pubitemid 27068593)
34. N. Huang, A. Dardis, and W.L. Miller Regulation of cytochrome b5 gene transcription by Sp3, GATA-6, and steroidogenic factor 1 in human adrenal NCI-H295A cells Mol. Endocrinol. 19 2005 2020 2034 (Pubitemid 41124198)
35. C.J. Lin, J.W. Martens, and W.L. Miller NF-1C, Sp1, and Sp3 are essential for transcription of the human gene for P450c17 (steroid 17alpha-hydroxylase/ 17, 20 lyase) in human adrenal NCI-H295A cells Mol. Endocrinol. 15 2001 1277 1293 (Pubitemid 32703477)
36. M.S. Butt, and M.T. Sultan Coffee and its consumption: benefits and risks Crit. Rev. Food Sci. Nutr. 51 2011 363 373
37. R.L. Brent, M.S. Christian, and R.M. Diener Evaluation of the reproductive and developmental risks of caffeine Birth Defects Res. B Dev. Reprod. Toxicol. 92 2011 152 187
38. P.R. Manna, M.T. Dyson, D.W. Eubank, B.J. Clark, E. Lalli, P. Sassone-Corsi, A.J. Zeleznik, and D.M. Stocco 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 (Pubitemid 34044507)
39. P.R. Manna, I.T. Huhtaniemi, X.J. Wang, D.W. Eubank, and D.M. Stocco Mechanisms of epidermal growth factor signaling: regulation of steroid biosynthesis and the steroidogenic acute regulatory protein in mouse Leydig tumor cells Biol. Reprod. 67 2002 1393 1404 (Pubitemid 35204914)
40. P.R. Manna, D.W. Eubank, E. Lalli, P. Sassone-Corsi, and D.M. Stocco 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 (Pubitemid 36722626)
41. J.T. Attwood, R.L. Yung, and B.C. Richardson DNA methylation and the regulation of gene transcription Cell. Mol. Life Sci. 59 2002 241 257 (Pubitemid 34169512)
42. J.I. Goodman, and R.E. Watson Altered DNA methylation: a secondary mechanism involved in carcinogenesis Annu. Rev. Pharmacol. Toxicol. 42 2002 501 525 (Pubitemid 34160534)
43. E. Li, C. Beard, and R. Jaenisch Role for DNA methylation in genomic imprinting Nature 366 1993 362 365 (Pubitemid 23349366)
44. D.B. Martinez-Arguelles, and V. Papadopoulos Epigenetic regulation of the expression of genes involved in steroid hormone biosynthesis and action Steroids 75 2010 467 476
45. E. Missaghian, P. Kempna, B. Dick, A. Hirsch, R. Ikhani-Koupaei, and B. Jegou Role of DNA methylation in the tissue-specific expression of the CYP17A1 gene for steroidogenesis in rodents J. Endocrinol. 202 2009 99 109
46. Q. Xue, Z. Lin, P. Yin, M.P. Milad, Y.H. Cheng, and E. Confino Transcriptional activation of steroidogenic factor-1 by hypomethylation of the 5′ CpG island in endometriosis J. Clin. Endocrinol. Metab. 92 2007 3261 3267 (Pubitemid 47236401)
47. J. Boyes, and A. Bird DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein Cell 64 1991 1123 1134 (Pubitemid 121001199)
48. K. Myant, and I. Stancheva LSH cooperates with DNA methyltransferases to repress transcription Mol. Cell. Biol. 28 2008 215 226
49. M. Comb, and H.M. Goodman CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2 Nucleic Acids Res. 18 1990 3975 3982
50. J. Kim, A. Kollhoff, A. Bergmann, and L. Stubbs Methylation-sensitive binding of transcription factor YY1 to an insulator sequence within the paternally expressed imprinted gene, Peg3 Hum. Mol. Genet. 12 2003 233 245 (Pubitemid 36204421)
51. T.H. Bestor Gene silencing. Methylation meets acetylation Nature 393 1998 311 312 (Pubitemid 28269689)
52. R. Murr Interplay between different epigenetic modifications and mechanisms Adv. Genet. 70 2010 101 141
53. C. Guerrero-Bosagna, M. Settles, B. Lucker, and M.K. Skinner Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome PLoS ONE 5 2010 e13100
54. D. Deng, Z. Liu, and Y. Du Epigenetic alterations as cancer diagnostic, prognostic, and predictive biomarkers Adv. Genet. 71 2010 125 176
55. F. Einstein, R.F. Thompson, T.D. Bhagat, M.J. Fazzari, A. Verma, N. Barzilai, and J.M. Greally Cytosine methylation dysregulation in neonates following intrauterine growth restriction PLoS ONE 5 2010 e8887
56. K.A. Lillycrop, E.S. Phillips, A.A. Jackson, M.A. Hanson, and G.C. Burdge Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring J. Nutr. 135 2005 1382 1386 (Pubitemid 40799599)