Smad3 is required for normal follicular follicle-stimulating hormone responsiveness in the mouse

Biology of Reproduction

Volumn 81, Issue 4, 2009, Pages 730-738

  Gong, Xiaoyan ^a   McGee, Elizabeth A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Fertility; Follicle stimulating hormone receptor; Folliculogenesis; Fshr; Mechanisms of hormone action; Ovary; Smad3

Indexed keywords

AROMATASE; FOLLITROPIN; FOLLITROPIN RECEPTOR; GONADOTROPIN; SMAD3 PROTEIN; SMAD3 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; ARTICLE; C57BL MOUSE; CELL CULTURE; FEMALE; GENE EXPRESSION; GENETICS; GRANULOSA CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; MOUSE; MOUSE MUTANT; OVARY; OVARY FOLLICLE; PHYSIOLOGY; PROMOTER REGION; SIGNAL TRANSDUCTION;

ANIMALS; AROMATASE; CELLS, CULTURED; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GONADOTROPINS; GRANULOSA CELLS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOSIS; OVARIAN FOLLICLE; OVARY; PROMOTER REGIONS, GENETIC; RECEPTORS, FSH; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 74049150498     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.070086     Document Type: Article

References (39)

1. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21: 200-214.
2. McGee EA, Perlas E, LaPolt PS, Tsafriri A, Hsueh AJ. Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biol Reprod 1997; 57: 990-998.
3. Adashi EY. With a little help from my friends: the evolving story of intraovarian regulation. Endocrinology 1995; 136: 4161-4162.
4. Knight PG, Glister C. TGF-β superfamily members and ovarian follicle development. Reproduction 2006; 132: 191-206.
5. Inoue K, Nakamura K, Abe K, Hirakawa T, Tsuchiya M, Oomori Y, Matsuda H, Miyamoto K, Minegishi T. Mechanisms of action of transforming growth factor beta on the expression of follicle-stimulating hormone receptor messenger ribonucleic acid levels in rat granulosa cells. Biol Reprod 2003; 69: 1238-1244.
6. Minegishi T, Kishi H, Tano M, Kameda T, Hirakawa T, Miyamoto K. Control of FSH receptor mRNA expression in rat granulosa cells by 3′,5′- cyclic adenosine monophosphate, activin, and follistatin. Mol Cell Endocrinol 1999; 149: 71-77.
7. Hayashi M, McGee EA, Min G, Klein C, Rose UM, van Duin M. Hsueh AJ. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 1999; 140: 1236-1244.
8. McGee EA, Smith R, Spears N, Nachtigal MW, Ingraham H, Hsueh AJ. Mullerian inhibitory substance induces growth of rat preantral ovarian follicles. Biol Reprod 2001; 64: 293-298.
9. Thomas FH, Armstrong DG, Telfer EE. Activin promotes oocyte development in ovine preantral follicles in vitro. Reprod Biol Endocrinol 2003; 1: 76-83.
10. Thomas FH, Ethier JF, Shimasaki S, Vanderhyden BC. Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 2005; 146: 941-949.
11. Wrana JL. Crossing Smads. Sci STKE 2000; 2000: eREl.
12. Xu J, Oakley J, McGee EA. Stage-specific expression of Smad2 and Smad3 during folliculogenesis. Biol Reprod 2002; 66: 1571-1578.
13. Tomic D, Brodie SG, Deng C, Hickey RJ, Babus JK, Malkas LH, Flaws JA. Smad 3 may regulate follicular growth in the mouse ovary. Biol Reprod 2002; 66: 917-923.
14. Tomic D, Miller KP, Kenny HA, Woodruff TK, Hoyer P, Flaws JA. Ovarian follicle development requires Smad3. Mol Endocrinol 2004; 18: 2224-2240.
15. Yang X, Letterio JJ, Leehleider RJ, Chen L, Hayman R, Gu H, Roberts AB, Deng C. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta;. Embryo J 1999; 18: 1280-1291.
16. Roberts AB, Russo A, Felici A, Flanders KC. Smad3: a key player in pathogenetic mechanisms dependent on TGF-β Ann N Y Acad Sci 2003; 995: 1-10.
17. Weinstein M, Yang X, Deng C. Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev 2000; 11: 49-58.
18. Nothnick WB, Soloway P, Curry TE Jr. Assessment of the role of tissue inhibitor of metalloproteinase-1 (TIMP-1) during the periovulatory period in female mice lacking a functional TIMP-1 gene. Biol Reprod 1997; 56: 1181-1188.
19. McGee EA, Chun SY, Lai S, He Y, Hsueh AJ. Keratinocyte growth factor promotes the survival, growth, and differentiation of preantral ovarian follicles. Fertil Steril 1999; 71: 732-738.
20. McGee E, Spears N, Minami S, Hsu SY, Chun SY, Billig H, Hsueh AJ. Preantral ovarian follicles in serum-free culture: suppression of apoptosis after activation of the cyclic guanosine 3′,5′-monophosphate pathway and stimulation of growth and differentiation by follicle-stimulating hormone. Endocrinology 1997; 138: 2417-2424.
21. Campbell KL. Ovarian granulosa cells isolated with EGTA and hypertonic sucrose: cellular integrity and function. Biol Reprod 1979; 21: 773-786.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C (T)) method. Methods 2001;25: 402-408.
23. Jung M, Ramankulov A, Roigas J, Johannsen M, Ringsdorf M, Kristiansen G, Jung K. In search of suitable reference genes for gene expression studies of human renal cell carcinoma by real-time PCR. BMC Mol Biol 2007; 8: e47.
24. Peluso JJ, Pappalardo A. Progesterone regulates granulosa cell viability through a protein kinase G-dependent mechanism that may involve 14-3-3sigma. Biol Reprod 2004; 71: 1870-1878.
25. Geles KG, Freiman RN, Liu WL, Zheng S, Voronina E, Tjian R. Cell-type-selective induction of c-jun by TAF4b directs ovarian-specific transcription networks. Proc Natl Acad Sci U S A 2006; 103: 2594-2599.
26. Stein LS, Stoica G, Tilley R, Burghardt RC. Rat ovarian granulosa cell culture: a model system for the study of cell-cell communication during multistep transformation. Cancer Res 1991; 51: 696-706.
27. Chipuk JE, Cornelius SC, Pultz NJ, Jorgensen JS, Bonham MJ, Kim SJ, Danielpour D. The androgen receptor represses transforming growth factor-beta signaling through interaction with Smad3. J Biol Chem 2002; 277: 1240-1248.
28. Sommers JP, DeLoia J, Zeleznik AJ. Adenovirus-directed expression of a nonphosphoryl table mutant of CREB (cAMP response element binding protein) adversely affects the survival, but not the differentiation, of rat granulosa cells. Mol Endocrinol 1999; 13: 1364-1372.
29. Murray A, Spears N. Follicular development in vitro. Semin Reprod Med 2000; 18: 109-122.
30. Gaytan F, Morales C, Bellido C, Aguilar E, Sancbez-Criado JE. Proliferative activity in the different ovarian compartments in cycling rats estimated by the 5-bromodeoxyuridine technique. Biol Reprod 1996; 54: 1356-1365.
31. Park Y, Maizeis ET, Feiger ZJ, Alam H, Peters CA, Woodruff TK, Unterman TG, Lee EJ, Jameson JL, Hunzicker-Dunn M. Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad. J Biol Chem 2005; 280: 9135-9148.
32. Zawel L, Dai J, Buckhaults P, Zhou S, Kinzler K, Vogelstein B, Kern SE. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1988; 1: 611-617.
33. Denissova N, Pouponnot C, Long J, He D, Liu F. Transforming growth factor β-inducible independent binding of SMAD to the Smad? promoter. Proc Natl Acad Sci U S A 2000; 97: 6397-6402.
34. Wu Y, Zhang X, Salmon M, Lin X, Zehner ZE. TGFbetal regulation of vimentin gene expression during differentiation of the C2C12 skeletal myogenic cell line requires Smads, Ap-1 and Spl family members. Biochim Biophys Acta 2007; 1773: 427-439.
35. Levallet J, Koskimies P, Rahman N, Huhtaniemi I. The promoter of murine follicle-stimulating hormone receptor: functional characterization and regulation by transcription factor steroidogenic factor 1. Mol Endocrinol 2001; 15: 80-92.
36. Looyenga BD, Hammer GD. Genetic removal of Smad3 from inhibin-null mice attenuates tumor progression by uncoupling extracellular mitogenic signals from the cell cycle machinery. Mol Endocrinol 2007; 10: 2440-2457.
37. Liu J, Aronow B, Witte DP, Pope WF, La Barbera A. Cyclic and maturation-dependent regulation of follicle-stimulating hormone receptor and luteinizing hormone receptor messenger ribonucleic acid expression in the porcine ovary. Biol Reprod 1998; 58: 648-658.
38. Massague J, Gomis RR. The logic of TGFbeta signaling. FEES Lett 2006: 580: 2811-2820.
39. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol 2008; 28: 7001-7011.