Prenatal nicotinic exposure suppresses fetal adrenal steroidogenesis via steroidogenic factor 1 (SF-1) deacetylation

Toxicology and Applied Pharmacology

Volumn 277, Issue 3, 2014, Pages 231-241

  Yan, You e ^a   Liu, Lian ^a,c   Wang, Jian fei ^a   Liu, Fang ^a   Li, Xiao hai ^a   Qin, Hai quan ^a   Wang, Hui ^a,b  

^a WUHAN UNIVERSITY   (China)

^b HUBEI PROVINCIAL KEY LABORATORY OF DEVELOPMENTALLY ORIGINATED DISEASE   (China)

^c YANGTZE UNIVERSITY   (China)

Author keywords

Histone deacetylation; Nicotine; Steroidogenesis; Steroidogenic factor 1

Indexed keywords

BISULFITE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CORTICOSTERONE; HISTONE DEACETYLASE 2; HISTONE H3; MESSENGER RNA; NICOTINE; STEROIDOGENIC FACTOR 1; TRICHOSTATIN A;

ACETYLATION; ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEACETYLATION; DNA METHYLATION; DNA MODIFICATION; EPIGENETICS; FEMALE; FETUS; FETUS WEIGHT; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INTRAUTERINE GROWTH RETARDATION; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRENATAL EXPOSURE; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN INTERACTION; STEROIDOGENESIS; WEIGHT REDUCTION; ZONA FASCICULATA;

RATTUS;

HISTONE DEACETYLATION; NICOTINE; STEROIDOGENESIS; STEROIDOGENIC FACTOR-1;

ADRENAL GLANDS; ANIMALS; CELL LINE; EPIGENOMICS; FEMALE; FETAL DEVELOPMENT; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MATERNAL EXPOSURE; NICOTINE; PREGNANCY; RATS; STEROIDOGENIC FACTOR 1;

EID: 84899958845     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.03.019     Document Type: Article

References (50)

1. Alkondon M., Pereira E.F., Almeida L.E., Randall W.R., Albuquerque E.X. Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 2000, 39:2726-2739.
2. Benowitz N.L., Jacob P. Daily intake of nicotine during cigarette smoking. Clin. Pharmacol. Ther. 1984, 35:499-504.
3. Chen W.Y., Juan L.J., Chung B.C. SF-1 (nuclear receptor 5A1) activity is activated by cyclic AMP via p300-mediated recruitment to active foci, acetylation, and increased DNA binding. Mol. Cell. Biol. 2005, 25:10442-10453.
4. Chen M., Wang T., Liao Z.X., Pan X.L., Feng Y.H., Wang H. Nicotine-induced prenatal overexposure to maternal glucocorticoid and intrauterine growth retardation in rat. Exp. Toxicol. Pathol. 2007, 59:245-251.
5. 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.
6. Dardis A., Miller W.L. Dexamethasone does not exert direct intracellular feedback on steroidogenesis in human adrenal NCI-H295A cells. J. Endocrinol. 2003, 179:131-142.
7. Dwyer J.B., Broide R.S., Leslie F.M. Nicotine and brain development. Birth Defects Res. C Embryol. Today 2008, 84:30-44.
8. Fantuzzi G., Aggazzotti G., Righi E., Facchinetti F., Bertucci E., Kanitz S., Barbone F., Sansebastiano G., Battaglia M.A., Leoni V., Fabiani L., Triassi M., Sciacca S. Preterm delivery and exposure to active and passive smoking during pregnancy: a case-control study from Italy. Paediatr. Perinat. Epidemiol. 2007, 21:194-200.
9. Fowden A.L., Forhead A.J. Endocrine mechanisms of intrauterine programming. Reproduction 2004, 127:515-526.
10. Grozinger C.M., Hassig C.A., Schreiber S.L. Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:4868-4873.
11. Hait N.C., Allegood J., Maceyka M., Strub G.M., Harikumar K.B., Singh S.K., Luo C., Marmorstein R., Kordula T., Milstien S., Spiegel S. Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 2009, 325:1254-1257.
12. Hammoud A.O., Bujold E., Sorokin Y., Schild C., Krapp M., Baumann P. Smoking in pregnancy revisited: findings from a large population-based study. Am. J. Obstet. Gynecol. 2005, 192:1856-1862. (discussion 1862-1853).
13. Harris A., Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 2011, 59:279-289.
14. Hoivik E.A., Aumo L., Aesoy R., Lillefosse H., Lewis A.E., Perrett R.M., Stallings N.R., Hanley N.A., Bakke M. Deoxyribonucleic acid methylation controls cell type-specific expression of steroidogenic factor 1. Endocrinology 2008, 149:5599-5609.
15. Hoivik E.A., Bjanesoy T.E., Mai O., Okamoto S., Minokoshi Y., Shima Y., Morohashi K., Boehm U., Bakke M. DNA methylation of intronic enhancers directs tissue-specific expression of steroidogenic factor 1/adrenal 4 binding protein (SF-1/Ad4BP). Endocrinology 2011, 152:2100-2112.
16. Hong C.Y., Park J.H., Ahn R.S., Im S.Y., Choi H.S., Soh J., Mellon S.H., Lee K. Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor alpha. Mol. Cell. Biol. 2004, 24:2593-2604.
17. Hood R.D. Developmental and Reproductive Toxicology: A Practical Approach 2011, Informa Healthcare, New York.
18. Jacob A.L., Lund J. Mutations in the activation function-2 core domain of steroidogenic factor-1 dominantly suppresses PKA-dependent transactivation of the bovine CYP17 gene. J. Biol. Chem. 1998, 273:13391-13394.
19. Jacob A.L., Lund J., Martinez P., Hedin L. Acetylation of steroidogenic factor 1 protein regulates its transcriptional activity and recruits the coactivator GCN5. J. Biol. Chem. 2001, 276:37659-37664.
20. Jordanov J.S. Cotinine concentrations in amniotic fluid and urine of smoking, passive smoking and non-smoking pregnant women at term and in the urine of their neonates on 1st day of life. Eur. J. Pediatr. 1990, 149:734-737.
21. Kraugerud M., Zimmer K.E., Dahl E., Berg V., Olsaker I., Farstad W., Ropstad E., Verhaegen S. 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. Toxic. Environ. Health A 2010, 73:1122-1132.
22. Lalli E., Ohe K., Hindelang C., Sassone-Corsi P. Orphan receptor DAX-1 is a shuttling RNA binding protein associated with polyribosomes via mRNA. Mol. Cell. Biol. 2000, 20:4910-4921.
23. Lan H.C., Li H.J., Lin G., Lai P.Y., Chung B.C. Cyclic AMP stimulates SF-1-dependent CYP11A1 expression through homeodomain-interacting protein kinase 3-mediated Jun N-terminal kinase and c-Jun phosphorylation. Mol. Cell. Biol. 2007, 27:2027-2036.
24. Landais E., El-Khoury V., Prevost A., Dufer J., Liautaud-Roger F. Nicotine induces chromatin changes and c-Jun up-regulation in HL-60 leukemia cells. Oncol. Rep. 2005, 14:1553-1558.
25. Lavoie H.A., King S.R. Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B. Exp. Biol. Med. (Maywood) 2009, 234:880-907.
26. Lucki N.C., Bandyopadhyay S., Wang E., Merrill A.H., Sewer M.B. Acid ceramidase (ASAH1) is a global regulator of steroidogenic capacity and adrenocortical gene expression. Mol. Endocrinol. 2012, 26:228-243.
27. Luo J., Su F., Chen D., Shiloh A., Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 2000, 408:377-381.
28. Mackay J. The making of a convention on tobacco control. Bull. World Health Organ. 2003, 81:551.
29. Manna P.R., Stocco D.M. Regulation of the steroidogenic acute regulatory protein expression: functional and physiological consequences. Curr. Drug Targets Immune Endocr. Metab. Disord. 2005, 5:93-108.
30. 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.
31. Mitchell E.A., Milerad J. Smoking and the sudden infant death syndrome. Rev. Environ. Health 2006, 21:81-103.
32. Oliveira E., Pinheiro C.R., Santos-Silva A.P., Trevenzoli I.H., Abreu-Villaca Y., Nogueira Neto J.F., Reis A.M., Passos M.C., Moura E.G., Lisboa P.C. Nicotine exposure affects mother's and pup's nutritional, biochemical, and hormonal profiles during lactation in rats. J. Endocrinol. 2010, 205:159-170.
33. Parker K.L., Schimmer B.P. Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 1997, 18:361-377.
34. Parker K.L., Rice D.A., Lala D.S., Ikeda Y., Luo X., Wong M., Bakke M., Zhao L., Frigeri C., Hanley N.A., Stallings N., Schimmer B.P. Steroidogenic factor 1: an essential mediator of endocrine development. Recent Prog. Horm. Res. 2002, 57:19-36.
35. Pastor V., Host L., Zwiller J., Bernabeu R. Histone deacetylase inhibition decreases preference without affecting aversion for nicotine. J. Neurochem. 2011, 116:636-645.
36. Pidoplichko V.I., DeBiasi M., Williams J.T., Dani J.A. Nicotine activates and desensitizes midbrain dopamine neurons. Nature 1997, 390:401-404.
37. Sanderson J.T. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals. Toxicol. Sci. 2006, 94:3-21.
38. Son H.J., Kim J.Y., Hahn Y., Seo S.B. Negative regulation of JAK2 by H3K9 methyltransferase G9a in leukemia. Mol. Cell. Biol. 2012, 32:3681-3694.
39. Sugawara T., Kiriakidou M., McAllister J.M., Holt J.A., Arakane F., Strauss J.F. Regulation of expression of the steroidogenic acute regulatory protein (StAR) gene: a central role for steroidogenic factor 1. Steroids 1997, 62:5-9.
40. Sugawara T., Sakuragi N., Minakami H. CREM confers cAMP responsiveness in human steroidogenic acute regulatory protein expression in NCI-H295R cells rather than SF-1/Ad4BP. J. Endocrinol. 2006, 191:327-337.
41. Tan Y., Liu J., Deng Y., Cao H., Xu D., Cu F., Lei Y., Magdalou J., Wu M., Chen L., Wang H. Caffeine-induced fetal rat over-exposure to maternal glucocorticoid and histone methylation of liver IGF-1 might cause skeletal growth retardation. Toxicol. Lett. 2012, 214:279-287.
42. Voutilainen R., Tapanainen J., Chung B.C., Matteson K.J., Miller W.L. Hormonal regulation of P450scc (20,22-desmolase) and P450c17 (17 alpha-hydroxylase/17,20-lyase) in cultured human granulosa cells. J. Clin. Endocrinol. Metab. 1986, 63:202-207.
43. Wang H., Huang M., Peng R.X., Le J. Influences of 3-methylcholanthrene, phenobarbital and dexamethasone on xenobiotic metabolizing-related cytochrome P450 enzymes and steroidogenesis in human fetal adrenal cortical cells. Acta Pharmacol. Sin. 2006, 27:1093-1096.
44. Wang H., Ping J., Peng R.X., Yue J., Xia X.Y., Li Q.X., Kong R., Hong J.Y. Changes of multiple biotransformation phase I and phase II enzyme activities in human fetal adrenals during fetal development. Acta Pharmacol. Sin. 2008, 29:231-238.
45. Wang T., Chen M., Liu L., Cheng H., Yan Y.E., Feng Y.H., Wang H. Nicotine induced CpG methylation of Pax6 binding motif in StAR promoter reduces the gene expression and cortisol production. Toxicol. Appl. Pharmacol. 2011, 257:328-337.
46. Warren C.W., Jones N.R., Eriksen M.P., Asma S. Patterns of global tobacco use in young people and implications for future chronic disease burden in adults. Lancet 2006, 367:749-753.
47. Wotus C., Levay-Young B.K., Rogers L.M., Gomez-Sanchez C.E., Engeland W.C. Development of adrenal zonation in fetal rats defined by expression of aldosterone synthase and 11beta-hydroxylase. Endocrinology 1998, 139:4397-4403.
48. Xu D., Liang G., Yan Y.E., He W.W., Liu Y.S., Chen L.B., Magdalou J., Wang H. Nicotine-induced over-exposure to maternal glucocorticoid and activated glucocorticoid metabolism causes hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic alterations in fetal rats. Toxicol. Lett. 2012, 209:282-290.
49. Xu D., Zhang B., Liang G., Ping J., Kou H., Li X., Xiong J., Hu D., Chen L., Magdalou J., Wang H. Caffeine-induced activated glucocorticoid metabolism in the hippocampus causes hypothalamic-pituitary-adrenal axis inhibition in fetal rats. PLoS One 2012, 7:e44497.
50. Yildiz D. Nicotine, its metabolism and an overview of its biological effects. Toxicon 2004, 43:619-632.