Effects of resveratrol on growth and function of rat ovarian granulosa cells

Fertility and Sterility

Volumn 98, Issue 6, 2012, Pages 1563-1573

  Ortega, Israel ^a,c   Wong, Donna H ^a   Villanueva, Jesus A ^a   Cress, Amanda B ^a   Sokalska, Anna ^a,d   Stanley, Scott D ^b   Duleba, Antoni J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c IVI Madrid   (Spain)

^d POZNAN UNIVERSITY OF MEDICAL SCIENCES   (Poland)

Author keywords

AMH; Apoptosis; granulosa cells; proliferation; resveratrol; steroidogenesis; VEGF

Indexed keywords

CASPASE 3; CASPASE 7; MUELLERIAN INHIBITING FACTOR; PROGESTERONE; RESVERATROL; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; AROMATIZATION; ARTICLE; CELL COUNT; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; FEMALE; GRANULOSA CELL; HORMONE SYNTHESIS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS; WESTERN BLOTTING;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GRANULOSA CELLS; RATS; RATS, SPRAGUE-DAWLEY; STILBENES;

EID: 84870341531     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2012.08.004     Document Type: Article

References (57)

1. J.A. Baur, and D.A. Sinclair Therapeutic potential of resveratrol: the in vivo evidence Nat Rev Drug Discov 5 2006 493 506 (Pubitemid 44136961)
2. M. Nassiri-Asl, and H. Hosseinzadeh Review of the pharmacological effects of Vitis vinifera (grape) and its bioactive compounds Phytotherapy research: PTR 23 2009 1197 1204
3. N. Labinskyy, A. Csiszar, G. Veress, G. Stef, P. Pacher, and G. Oroszi Vascular dysfunction in aging: potential effects of resveratrol, an antiinflammatory phytoestrogen Curr Med Chem 13 2006 989 996
4. S.V. Penumathsa, and N. Maulik Resveratrol: a promising agent in promoting cardioprotection against coronary heart disease Can J Physiol Pharmacol 87 2009 275 286
5. S. Yousuf, F. Atif, M. Ahmad, N. Hoda, T. Ishrat, and B. Khan Resveratrol exerts its neuroprotective effect by modulating mitochondrial dysfunctions and associated cell death during cerebral ischemia Brain Res 1250 2009 242 253
6. M. Athar, J.H. Back, L. Kopelovich, D.R. Bickers, and A.L. Kim Multiple molecular targets of resveratrol: anti-carcinogenic mechanisms Arch Biochem Biophys 486 2009 95 102
7. D.H. Wong, J.A. Villanueva, A.B. Cress, and A.J. Duleba Effects of resveratrol on proliferation and apoptosis in rat ovarian theca-interstitial cells Mol Hum Reprod 16 2010 251 259
8. D.H. Wong, J.A. Villanueva, A.B. Cress, A. Sokalska, I. Ortega, and A.J. Duleba Resveratrol inhibits the mevalonate pathway and potentiates the antiproliferative effects of simvastatin in rat theca-interstitial cells Fertil Steril 96 2011 1252 1258
9. R. Azziz, K.S. Woods, R. Reyna, T.J. Key, E.S. Knochenhauer, and B.O. Yildiz The prevalence and features of the polycystic ovary syndrome in an unselected population J Clin Endocrinol Metab 89 2004 2745 2749 (Pubitemid 38766360)
10. Peitsidis P, Agrawal R. Role of vascular endothelial growth factor in women with PCO and PCOS: a systematic review. Reprod Biomed Online 2010;20:444-52.
11. H. Yada, K. Hosokawa, K. Tajima, Y. Hasegawa, and F. Kotsuji Role of ovarian theca and granulosa cell interaction in hormone production and cell growth during the bovine follicular maturation process Biol Reprod 61 1999 1480 1486
12. M. Das, O. Djahanbakhch, B. Hacihanefioglu, E. Saridogan, M. Ikram, and L. Ghali Granulosa cell survival and proliferation are altered in polycystic ovary syndrome J Clin Endocrinol Metab 93 2008 881 887 (Pubitemid 351398567)
13. G.F. Erickson, D.A. Magoffin, J.R. Cragun, and R.J. Chang The effects of insulin and insulin-like growth factors-I and -II on estradiol production by granulosa cells of polycystic ovaries J Clin Endocrinol Metab 70 1990 894 902
14. P. Pigny, E. Merlen, Y. Robert, C. Cortet-Rudelli, C. Decanter, and S. Jonard Elevated serum level of antimullerian hormone in patients with polycystic ovary syndrome: relationship to the ovarian follicle excess and to the follicular arrest J Clin Endocrinol Metab 88 2003 5957 5962 (Pubitemid 38033078)
15. A.L. Durlinger, J.A. Visser, and A.P. Themmen Regulation of ovarian function: the role of anti-mullerian hormone Reproduction 124 2002 601 609 (Pubitemid 35402334)
16. L. Pellatt, L. Hanna, M. Brincat, R. Galea, H. Brain, and S. Whitehead Granulosa cell production of anti-mullerian hormone is increased in polycystic ovaries J Clin Endocrinol Metab 92 2007 240 245 (Pubitemid 46067538)
17. H.Y. Fan, M. Shimada, Z. Liu, N. Cahill, N. Noma, and Y. Wu Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation Development 135 2008 2127 2137 (Pubitemid 352015147)
18. J.R. Schreiber, K. Nakamura, and G.F. Erickson Progestins inhibit FSH-stimulated steroidogenesis in cultured rat granulosa cells Mol Cell Endocrinol 19 1980 165 173 (Pubitemid 10039842)
19. C. Wang, A.J. Hsueh, and G.F. Erickson LH stimulation of estrogen secretion by cultured rat granulosa cells Mol Cell Endocrinol 24 1981 17 28 (Pubitemid 11020451)
20. I. Ortega, A.B. Cress, D.H. Wong, J.A. Villanueva, A. Sokalska, and B.C. Moeller Simvastatin reduces steroidogenesis by inhibiting Cyp17a1 gene expression in rat ovarian theca-interstitial cells Biol Reprod 86 2012 1 9
21. Y. Yamazaki, M. Tsuruga, D. Zhou, Y. Fujita, X. Shang, and Y. Dang Cytoskeletal disruption accelerates caspase-3 activation and alters the intracellular membrane reorganization in DNA damage-induced apoptosis Exp Cell Res 259 2000 64 78
22. S.R. White, P. Williams, K.R. Wojcik, S. Sun, P.S. Hiemstra, and K.F. Rabe Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells Am J Respir Cell Mol Biol 24 2001 282 294 (Pubitemid 32228376)
23. I. Czajka-Oraniec, and E.R. Simpson Aromatase research and its clinical significance Endokrynol Pol 61 2010 126 134
24. S. Fulda, and K.M. Debatin Resveratrol modulation of signal transduction in apoptosis and cell survival: a mini-review Cancer Detect Prev 30 2006 217 223 (Pubitemid 44163050)
25. K. Iijima, M. Yoshizumi, M. Hashimoto, S. Kim, M. Eto, and J. Ako Red wine polyphenols inhibit proliferation of vascular smooth muscle cells and downregulate expression of cyclin A gene Circulation 101 2000 805 811 (Pubitemid 30100089)
26. N. Kawada, S. Seki, M. Inoue, and T. Kuroki Effect of antioxidants, resveratrol, quercetin, and N-acetylcysteine, on the functions of cultured rat hepatic stellate cells and Kupffer cells Hepatology 27 1998 1265 1274 (Pubitemid 28227853)
27. M. Alkhalaf, and S. Jaffal Potent antiproliferative effects of resveratrol on human osteosarcoma SJSA1 cells: novel cellular mechanisms involving the ERKs/p53 cascade Free Radic Biol Med 41 2006 318 325 (Pubitemid 43928507)
28. J. Cui, R. Sun, Y. Yu, S. Gou, G. Zhao, and C. Wang Antiproliferative effect of resveratrol in pancreatic cancer cells Phytother Res 24 2010 1637 1644
29. Y.A. Kim, S.H. Rhee, K.Y. Park, and Y.H. Choi Antiproliferative effect of resveratrol in human prostate carcinoma cells J Med Food 6 2003 273 280 (Pubitemid 38114319)
30. M. Fontecave, M. Lepoivre, E. Elleingand, C. Gerez, and O. Guittet Resveratrol, a remarkable inhibitor of ribonucleotide reductase FEBS Lett 421 1998 277 279 (Pubitemid 28045770)
31. N.J. Sun, S.H. Woo, J.M. Cassady, and R.M. Snapka DNA polymerase and topoisomerase II inhibitors from Psoralea corylifolia J Nat Prod 61 1998 362 366 (Pubitemid 28160726)
32. F.D. Ragione, V. Cucciolla, A. Borriello, V.D. Pietra, L. Racioppi, and G. Soldati Resveratrol arrests the cell division cycle at S/G2 phase transition Biochem Biophys Res Commun 250 1998 53 58 (Pubitemid 28448621)
33. Y. Schneider, F. Vincent, B. Duranton, L. Badolo, F. Gosse, and C. Bergmann Anti-proliferative effect of resveratrol, a natural component of grapes and wine, on human colonic cancer cells Cancer Lett 158 2000 85 91 (Pubitemid 30627485)
34. N. Kuwajerwala, E. Cifuentes, S. Gautam, M. Menon, E.R. Barrack, and G.P. Reddy Resveratrol induces prostate cancer cell entry into s phase and inhibits DNA synthesis Cancer Res 62 2002 2488 2492 (Pubitemid 34462723)
35. S. Elmore Apoptosis: a review of programmed cell death Toxicol Pathol 35 2007 495 516 (Pubitemid 46911891)
36. G.M. Cohen Caspases: the executioners of apoptosis Biochem J 326 Pt 1 1997 1 16 (Pubitemid 27386911)
37. C.K. Singh, A. Kumar, D.B. Hitchcock, D. Fan, R. Goodwin, and H.A. Lavoie Resveratrol prevents embryonic oxidative stress and apoptosis associated with diabetic embryopathy and improves glucose and lipid profile of diabetic dam Mol Nutr Food Res 55 2011 1186 1196
38. M. MacCarrone, T. Lorenzon, P. Guerrieri, and A.F. Agro Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity Eur J Biochem 265 1999 27 34 (Pubitemid 29466009)
39. M.V. Clement, J.L. Hirpara, S.H. Chawdhury, and S. Pervaiz Chemopreventive agent resveratrol, a natural product derived from grapes, triggers CD95 signaling-dependent apoptosis in human tumor cells Blood 92 1998 996 1002 (Pubitemid 28355484)
40. T.C. Hsieh, and J.M. Wu Differential effects on growth, cell cycle arrest, and induction of apoptosis by resveratrol in human prostate cancer cell lines Exp Cell Res 249 1999 109 115 (Pubitemid 29394029)
41. J.J. Eppig Oocyte control of ovarian follicular development and function in mammals Reproduction 122 2001 829 838 (Pubitemid 33138562)
42. R.B. Gilchrist, L.J. Ritter, S. Myllymaa, N. Kaivo-Oja, R.A. Dragovic, and T.E. Hickey Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation J Cell Sci 119 2006 3811 3821 (Pubitemid 44614433)
43. J.J. Eppig, K. Wigglesworth, and F.L. Pendola The mammalian oocyte orchestrates the rate of ovarian follicular development Proc Natl Acad Sci U S A 99 2002 2890 2894 (Pubitemid 34240556)
44. S.G. Hillier, P.F. Whitelaw, and C.D. Smyth Follicular oestrogen synthesis: the "two-cell, two-gonadotrophin" model revisited Mol Cell Endocrinol 100 1994 51 54 (Pubitemid 24109526)
45. Y. Wang, and L.K. Leung Pharmacological concentration of resveratrol suppresses aromatase in JEG-3 cells Toxicol Lett 173 2007 175 180 (Pubitemid 47391550)
46. Y. Wang, K.W. Lee, F.L. Chan, S. Chen, and L.K. Leung The red wine polyphenol resveratrol displays bilevel inhibition on aromatase in breast cancer cells Toxicol Sci 92 2006 71 77 (Pubitemid 43985791)
47. S.A. Whitehead, and M. Lacey Phytoestrogens inhibit aromatase but not 17beta-hydroxysteroid dehydrogenase (HSD) type 1 in human granulosa-luteal cells: evidence for FSH induction of 17beta-HSD Hum Reprod 18 2003 487 494 (Pubitemid 36329312)
48. S. Rice, H.D. Mason, and S.A. Whitehead Phytoestrogens and their low dose combinations inhibit mRNA expression and activity of aromatase in human granulosa-luteal cells J Steroid Biochem Mol Biol 101 2006 216 225 (Pubitemid 44592638)
49. G. Basini, C. Tringali, L. Baioni, S. Bussolati, C. Spatafora, and F. Grasselli Biological effects on granulosa cells of hydroxylated and methylated resveratrol analogues Mol Nutr Food Res 54 Suppl 2 2010 S236 S243
50. R.R. Behringer, M.J. Finegold, and R.L. Cate Mullerian-inhibiting substance function during mammalian sexual development Cell 79 1994 415 425
51. W.M. Baarends, J.W. Hoogerbrugge, M. Post, J.A. Visser, D.G. de Rooij, and M. Parvinen Antimullerian hormone and antimullerian hormone type II receptor messenger ribonucleic acid expression during postnatal testis development and in the adult testis of the rat Endocrinology 136 1995 5614 5622
52. B.R. Kamat, L.F. Brown, E.J. Manseau, D.R. Senger, and H.F. Dvorak Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development Am J Pathol 146 1995 157 165
53. A. Villasante, A. Pacheco, A. Ruiz, A. Pellicer, and J.A. Garcia-Velasco Vascular endothelial cadherin regulates vascular permeability: implications for ovarian hyperstimulation syndrome J Clin Endocrinol Metab 92 2007 314 321 (Pubitemid 46067549)
54. R. Yang, H. Zhang, and L. Zhu Inhibitory effect of resveratrol on the expression of the VEGF gene and proliferation in renal cancer cells Mol Med Report 4 2011 981 983
55. H.B. Yu, H.F. Zhang, X. Zhang, D.Y. Li, H.Z. Xue, and C.E. Pan Resveratrol inhibits VEGF expression of human hepatocellular carcinoma cells through a NF-kappa B-mediated mechanism Hepatogastroenterology 57 2010 1241 1249
56. V. Trapp, B. Parmakhtiar, V. Papazian, L. Willmott, and J.P. Fruehauf Anti-angiogenic effects of resveratrol mediated by decreased VEGF and increased TSP1 expression in melanoma-endothelial cell co-culture Angiogenesis 13 2010 305 315
57. S.A. Stubbs, J. Stark, S.M. Dilworth, S. Franks, and K. Hardy Abnormal preantral folliculogenesis in polycystic ovaries is associated with increased granulosa cell division J Clin Endocrinol Metab 92 2007 4418 4426 (Pubitemid 350074765)