Trans-resveratrol inhibits phosphorylation of Smad2/3 and represses FSHβ gene expression by a SirT1-independent pathway in LβT2 gonadotrope cells

Reproductive Toxicology

Volumn 32, Issue 1, 2011, Pages 85-92

  Lan, Debin ^b   Lu, Min ^b   Sharma, Shweta ^b   Mellon, Pamela L ^b   Olefsky, Jerrold M ^b   Webster, Nicholas J G ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

FSH; Repression; Resveratrol; Smad2 3

Indexed keywords

ACTIVIN; FOLLITROPIN BETA SUBUNIT; PROTEIN P53; RESVERATROL; SIRTUIN 1; SMAD2 PROTEIN; SMAD3 PROTEIN;

ACETYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FSH BETA GENE; GENE; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GONADOTROPIN SECRETING CELL; LH BETA GENE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTIOXIDANTS; CELL LINE; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GENE EXPRESSION; GENE EXPRESSION PROFILING; GONADOTROPHS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; RNA, MESSENGER; SIRTUIN 1; SMAD2 PROTEIN; SMAD3 PROTEIN; STILBENES;

EID: 79960442457     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.05.006     Document Type: Article

References (42)

1. Baur J.A., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006, 444:337-342.
2. Okawara M., Katsuki H., Kurimoto E., Shibata H., Kume T., Akaike A. Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochem Pharmacol 2007, 73:550-560.
3. Sharma S., Anjaneyulu M., Kulkarni S.K., Chopra K. Resveratrol, a polyphenolic phytoalexin, attenuates diabetic nephropathy in rats. Pharmacology 2006, 76:69-75.
4. Milne J.C., Lambert P.D., Schenk S., Carney D.P., Smith J.J., Gagne D.J., et al. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 2007, 450:712-716.
5. Penumathsa S.V., Maulik N. Resveratrol: a promising agent in promoting cardioprotection against coronary heart disease. Can J Physiol Pharmacol 2009, 87:275-286.
6. Chaudhary N., Pfluger P.T. Metabolic benefits from Sirt1 and Sirt1 activators. Curr Opin Clin Nutr Metab Care 2009, 12:431-437.
7. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
8. Allard J.S., Heilbronn L.K., Smith C., Hunt N.D., Ingram D.K., Ravussin E., et al. In vitro cellular adaptations of indicators of longevity in response to treatment with serum collected from humans on calorie restricted diets. PLoS One 2008, 3:e3211.
9. Pacholec M., Bleasdale J.E., Chrunyk B., Cunningham D., Flynn D., Garofalo R.S., et al. SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 2010, 285:8340-8351.
10. Beher D., Wu J., Cumine S., Kim K.W., Lu S.C., Atangan L., et al. Resveratrol is not a direct activator of SIRT1 enzyme activity. Chem Biol Drug Des 2009, 74:619-624.
11. Dasgupta B., Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA 2007, 104:7217-7222.
12. Hardie D.G. AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 2008, 32(Suppl. 4):S7-12.
13. Stewart J.R., O'Brian C.A. Resveratrol antagonizes EGFR-dependent Erk1/2 activation in human androgen-independent prostate cancer cells with associated isozyme-selective PKC alpha inhibition. Invest New Drugs 2004, 22:107-117.
14. Szewczuk L.M., Forti L., Stivala L.A., Penning T.M. Resveratrol is a peroxidase-mediated inactivator of COX-1 but not COX-2: a mechanistic approach to the design of COX-1 selective agents. J Biol Chem 2004, 279:22727-22737.
15. Kennedy A., Overman A., Lapoint K., Hopkins R., West T., Chuang C.C., et al. Conjugated linoleic acid-mediated inflammation and insulin resistance in human adipocytes are attenuated by resveratrol. J Lipid Res 2009, 50:225-232.
16. Kang O.H., Jang H.J., Chae H.S., Oh Y.C., Choi J.G., Lee Y.S., et al. Anti-inflammatory mechanisms of resveratrol in activated HMC-1 cells: pivotal roles of NF-kappaB and MAPK. Pharmacol Res 2009, 59:330-337.
17. Aquilano K., Baldelli S., Rotilio G., Ciriolo M.R. trans-Resveratrol inhibits H2O2-induced adenocarcinoma gastric cells proliferation via inactivation of MEK1/2-ERK1/2-c-Jun signalling axis. Biochem Pharmacol 2009, 77:337-347.
18. Bowers J.L., Tyulmenkov V.V., Jernigan S.C., Klinge C.M. Resveratrol acts as a mixed agonist/antagonist for estrogen receptors alpha and beta. Endocrinology 2000, 141:3657-3667.
19. Gehm B.D., McAndrews J.M., Chien P.Y., Jameson J.L. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc Natl Acad Sci USA 1997, 94:14138-14143.
20. Sevov M., Elfineh L., Cavelier L.B. Resveratrol regulates the expression of LXR-alpha in human macrophages. Biochem Biophys Res Commun 2006, 348:1047-1054.
21. Lu M., Tang Q., Olefsky J.M., Mellon P.L., Webster N.J. Adiponectin activates adenosine monophosphate-activated protein kinase and decreases luteinizing hormone secretion in LbetaT2 gonadotropes. Mol Endocrinol 2008, 22:760-771.
22. Sharma S, Sharma PM, Mistry DS, Chang RJ, Olefsky JM, Mellon PL, et al. PPARG regulates gonadotropin-releasing hormone signaling in LbetaT2 cells in vitro and pituitary gonadotroph function in vivo in mice. Biol Reprod.
23. Solomon J.M., Pasupuleti R., Xu L., McDonagh T., Curtis R., DiStefano P.S., et al. Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Mol Cell Biol 2006, 26:28-38.
24. Bernard D.J. Both SMAD2 and SMAD3 mediate activin-stimulated expression of the follicle-stimulating hormone beta subunit in mouse gonadotrope cells. Mol Endocrinol 2004, 18:606-623.
25. Tu A.W., Luo K. Acetylation of Smad2 by the co-activator p300 regulates activin and transforming growth factor beta response. J Biol Chem 2007, 282:21187-21196.
26. Nakao A., Afrakhte M., Moren A., Nakayama T., Christian J.L., Heuchel R., et al. Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 1997, 389:631-635.
27. Bilezikjian L.M., Corrigan A.Z., Blount A.L., Chen Y., Vale W.W. Regulation and actions of Smad7 in the modulation of activin, inhibin, and transforming growth factor-beta signaling in anterior pituitary cells. Endocrinology 2001, 142:1065-1072.
28. Zhu X., Topouzis S., Liang L.F., Stotish R.L. Myostatin signaling through Smad2, Smad3 and Smad4 is regulated by the inhibitory Smad7 by a negative feedback mechanism. Cytokine 2004, 26:262-272.
29. Singh M, Parent S, Leblanc V, Asselin E. Resveratrol modulates the expression of PTGS2 and cellular proliferation in the normal rat endometrium in an AKT-dependent manner. Biol Reprod.
30. Jang J.Y., Park D., Shin S., Jeon J.H., Choi B.I., Joo S.S., et al. Antiteratogenic effect of resveratrol in mice exposed in utero to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Eur J Pharmacol 2008, 591:280-283.
31. Singh CK, Kumar A, Hitchcock DB, Fan D, Goodwin R, Lavoie HA, et al. Resveratrol prevents embryonic oxidative stress and apoptosis associated with diabetic embryopathy and improves glucose and lipid profile of diabetic dam. Mol Nutr Food Res.
32. Sato M., Pei R.J., Yuri T., Danbara N., Nakane Y., Tsubura A. Prepubertal resveratrol exposure accelerates N-methyl-N-nitrosourea-induced mammary carcinoma in female Sprague-Dawley rats. Cancer Lett 2003, 202:137-145.
33. Kyselova V., Peknicova J., Buckiova D., Boubelik M. Effects of p-nonylphenol and resveratrol on body and organ weight and in vivo fertility of outbred CD-1 mice. Reprod Biol Endocrinol 2003, 1:30.
34. Collodel G, Federico MG, Geminiani M, Martini S, Bonechi C, Rossi C, et al. Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod Toxicol.
35. Jiang Y.G., Peng T., Luo Y., Li M.C., Lin Y.H. Resveratrol reestablishes spermatogenesis after testicular injury in rats caused by 2,5-hexanedione. Chin Med J (Engl) 2008, 121:1204-1209.
36. Henry L.A., Witt D.M. Effects of neonatal resveratrol exposure on adult male and female reproductive physiology and behavior. Dev Neurosci 2006, 28:186-195.
37. Suchankova G., Nelson L.E., Gerhart-Hines Z., Kelly M., Gauthier M.S., Saha A.K., et al. Concurrent regulation of AMP-activated protein kinase and SIRT1 in mammalian cells. Biochem Biophys Res Commun 2009, 378:836-841.
38. Breen D.M., Sanli T., Giacca A., Tsiani E. Stimulation of muscle cell glucose uptake by resveratrol through sirtuins and AMPK. Biochem Biophys Res Commun 2008, 374:117-122.
39. McBurney M.W., Yang X., Jardine K., Hixon M., Boekelheide K., Webb J.R., et al. The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol Cell Biol 2003, 23:38-54.
40. Bordone L., Cohen D., Robinson A., Motta M.C., van Veen E., Czopik A., et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 2007, 6:759-767.
41. Wang F., Tong Q. SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1's repressive interaction with PPARgamma. Mol Biol Cell 2009, 20:801-808.
42. Pillai V.B., Sundaresan N.R., Kim G., Gupta M., Rajamohan S.B., Pillai J.B., et al. Exogenous NAD blocks cardiac hypertrophic response via activation of the SIRT3-LKB1-AMPK pathway. J Biol Chem 2009.