Transforming growth factor-β signaling participates in the maintenance of the primordial follicle pool in the mouse ovary

Journal of Biological Chemistry

Volumn 289, Issue 12, 2014, Pages 8299-8311

  Wang, Zheng Pin ^a   Mu, Xin Yi ^a,b   Guo, Meng ^a,c   Wang, Yi Jing ^a   Teng, Zhen ^a   Mao, Guan Ping ^a   Niu, Wan Bao ^a   Feng, Li Zhao ^a   Zhao, Li Hua ^a   Xia, Guo Liang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

^c CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; LAKES; MAMMALS; PHYSIOLOGY; SIGNALING;

GRANULOSA CELLS; MAMMALIAN TARGET; MORPHOLOGICAL ANALYSIS; PHOSPHATIDYLINOSITOL 3-KINASE; PHYSIOLOGICAL ROLES; SPECIFIC INHIBITORS; TRANSFORMING GROWTH FACTOR BETA; TUBEROUS SCLEROSIS;

POPULATION STATISTICS;

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN S6; S6 KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHRL1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; FETUS; GENE; GENE EXPRESSION REGULATION; GRANULOSA CELL; GROWTH REGULATION; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE; PRIORITY JOURNAL; TGF BETA R1 GENE; WESTERN BLOTTING;

CELL GROWTH; MOUSE; OOCYTE; OVARY; TRANSFORMING GROWTH FACTOR-Β (TGFΒ);

ANIMALS; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MULTIPROTEIN COMPLEXES; OOCYTES; ORGAN CULTURE TECHNIQUES; OVARIAN FOLLICLE; OVARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84896992713     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.532952     Document Type: Article

References (46)

1. Pepling, M. E. (2006) From primordial germ cell to primordial follicle. Mammalian female germ cell development. Genesis 44, 622-632
2. Pepling, M. E., and Spradling, A. C. (2001) Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol. 234, 339-351 (Pubitemid 32552663)
3. Bristol-Gould, S. K., Kreeger, P. K., Selkirk, C. G., Kilen, S. M., Cook, R. W., Kipp, J. L., Shea, L. D., Mayo, K. E., and Woodruff, T. K. (2006) Postnatal regulation of germ cells by activin. The establishment of the initial follicle pool. Dev. Biol. 298, 132-148 (Pubitemid 44414802)
4. Trombly, D. J., Woodruff, T. K., and Mayo, K. E. (2009) Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 150, 1014-1024
5. McGee, E. A., and Hsueh, A. J. (2000) Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200-214 (Pubitemid 32275595)
6. Broekmans, F. J., Knauff, E. A., te Velde, E. R., Macklon, N. S., and Fauser, B. C. (2007) Female reproductive ageing. Current knowledge and future trends. Trends Endocrinol. Metab. 18, 58-65 (Pubitemid 46275460)
7. Anderson, L. D., and Hirshfield, A. N. (1992) An overview of follicular development in the ovary. From embryo to the fertilized ovum in vitro. Md. Med. J. 41, 614-620
8. Myers, M., Middlebrook, B. S., Matzuk, M. M., and Pangas, S. A. (2009) Loss of inhibin α uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis. Dev. Biol. 334, 458-467
9. Hayashi, M., McGee, E. A., Min, G., Klein, C., Rose, U. M., van Duin, M., and Hsueh, A. J. (1999) Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140, 1236-1244 (Pubitemid 29104226)
10. Nilsson, E. E., and Skinner, M. K. (2002) Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol. Reprod. 67, 1018-1024 (Pubitemid 34925226)
11. Liu, L., Rajareddy, S., Reddy, P., Du, C., Jagarlamudi, K., Shen, Y., Gunnarsson, D., Selstam, G., Boman, K., and Liu, K. (2007) Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 134, 199-209 (Pubitemid 46152720)
12. John, G. B., Shirley, L. J., Gallardo, T. D., and Castrillon, D. H. (2007) Specificity of the requirement for Foxo3 in primordial follicle activation. Reproduction 133, 855-863 (Pubitemid 47162577)
13. Castrillon, D. H., Miao, L., Kollipara, R., Horner, J. W., and DePinho, R. A. (2003) Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301, 215-218 (Pubitemid 36858475)
14. John, G. B., Gallardo, T. D., Shirley, L. J., and Castrillon, D. H. (2008) Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev. Biol. 321, 197-204
15. Reddy, P., Liu, L., Adhikari, D., Jagarlamudi, K., Rajareddy, S., Shen, Y., Du, C., Tang, W., Hämäläinen, T., Peng, S. L., Lan, Z. J., Cooney, A. J., Huhtaniemi, I., and Liu, K. (2008) Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319, 611- 613
16. Adhikari, D., Flohr, G., Gorre, N., Shen, Y., Yang, H., Lundin, E., Lan, Z., Gambello, M. J., and Liu, K. (2009) Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol. Hum. Reprod. 15, 765-770
17. Adhikari, D., Zheng, W., Shen, Y., Gorre, N., Hämäläinen, T., Cooney, A. J., Huhtaniemi, I., Lan, Z. J., and Liu, K. (2010) Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum. Mol. Genet. 19, 397-410
18. Shull, M. M., and Doetschman, T. (1994) Transforming growth factor-β1 in reproduction and development. Mol. Reprod. Dev. 39, 239-246 (Pubitemid 24312168)
19. Ingman, W. V., and Robertson, S. A. (2002) Defining the actions of transforming growth factor β in reproduction. Bioessays 24, 904-914 (Pubitemid 35180845)
20. Godkin, J. D., and Doré, J. J. (1998) Transforming growth factor β and the endometrium. Rev. Reprod. 3, 1-6
21. Heldin, C. H., Miyazono, K., and ten Dijke, P. (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471 (Pubitemid 28013118)
22. Drummond, A. E. (2005) TGFbeta signalling in the development of ovarian function. Cell Tissue Res. 322, 107-115
23. Kaivo-oja, N., Jeffery, L. A., Ritvos, O., and Mottershead, D. G. (2006) Smad signalling in the ovary. Reprod. Biol. Endocrinol. 4, 21
24. Guéripel, X., Benahmed, M., and Gougeon, A. (2004) Sequential gonadotropin treatment of immature mice leads to amplification of transforming growth factor β action, via up-regulation of receptor-type 1, Smad 2 and 4, and down-regulation of Smad 6. Biol. Reprod. 70, 640-648 (Pubitemid 38233701)
25. Rosairo, D., Kuyznierewicz, I., Findlay, J., and Drummond, A. (2008) Transforming growth factor-β. Its role in ovarian follicle development. Reproduction 136, 799-809
26. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N., and Groffen, J. (1995) Abnormal lung development and cleft palate in mice lacking TGF-β3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet. 11, 415-421
27. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L., and Doetschman, T. (1997) TGFβ2 knockout mice have multiple developmental defects that are non-overlapping with other TGFβ knockout phenotypes. Development 124, 2659-2670 (Pubitemid 27341765)
28. Ingman, W. V., Robker, R. L., Woittiez, K., and Robertson, S. A. (2006) Null mutation in transforming growth factor β1 disrupts ovarian function and causes oocyte incompetence and early embryo arrest. Endocrinology 147, 835-845 (Pubitemid 43113001)
29. Schindler, R., Nilsson, E., and Skinner, M. K. (2010) Induction of ovarian primordial follicle assembly by connective tissue growth factor CTGF. PLoS One 5, e12979
30. Wang, H. B., Xia, G. L., Wang, Q., Li, M. L., and Lu, Z. X. (2001) Follicles were reconstituted from dissociated mouse fetal ovarian cells in vitro. Chinese Sci. Bull. 46, 672-674 (Pubitemid 32524979)
31. Uhl, M., Aulwurm, S., Wischhusen, J., Weiler, M., Ma, J. Y., Almirez, R., Mangadu, R., Liu, Y. W., Platten, M., Herrlinger, U., Murphy, A., Wong, D. H., Wick, W., Higgins, L. S., and Weller, M. (2004) SD-208, a novel transforming growth factor β receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res. 64, 7954-7961 (Pubitemid 39446929)
32. Flaws, J. A., Hirshfield, A. N., Hewitt, J. A., Babus, J. K., and Furth, P. A. (2001) Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol. Reprod. 64, 1153-1159 (Pubitemid 32239186)
33. Parrott, J. A., and Skinner, M. K. (1999) Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 140, 4262-4271 (Pubitemid 30647125)
34. T) method. Methods 25, 402-408 (Pubitemid 34164012)
35. Reddy, P., Adhikari, D., Zheng, W., Liang, S., Hämäläinen, T., Tohonen, V., Ogawa, W., Noda, T., Volarevic, S., Huhtaniemi, I., and Liu, K. (2009) PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum. Mol. Genet. 18, 2813-2824
36. Adhikari, D., Risal, S., Liu, K., and Shen, Y. (2013) Pharmacological inhibition of mTORC1 prevents over-activation of the primordial follicle pool in response to elevated PI3K signaling. PLoS One 8, e53810
37. Knecht, M., Feng, P., and Catt, K. (1987) Bifunctional role of transforming growth factor-β during granulosa cell development. Endocrinology 120, 1243-1249 (Pubitemid 17053974)
38. Li, Q., Agno, J. E., Edson, M. A., Nagaraja, A. K., Nagashima, T., and Matzuk, M. M. (2011) Transforming growth factor β receptor type 1 is essential for female reproductive tract integrity and function. PLoS Genet. 7, e1002320
39. Baarends, W. M., Uilenbroek, J. T., Kramer, P., Hoogerbrugge, J. W., van Leeuwen, E. C., Themmen, A. P., and Grootegoed, J. A. (1995) Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 136, 4951-4962
40. Runyan, C. E., Schnaper, H. W., and Poncelet, A. C. (2004) The phosphatidylinositol 3-kinase/Akt pathway enhances Smad3-stimulated mesangial cell collagen I expression in response to transforming growth factor-β1. J. Biol. Chem. 279, 2632-2639 (Pubitemid 38114250)
41. Bakin, A. V., Tomlinson, A. K., Bhowmick, N. A., Moses, H. L., and Arteaga, C. L. (2000) Phosphatidylinositol 3-kinase function is required for transforming growth factor β-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem. 275, 36803-36810 (Pubitemid 32002090)
42. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a forkhead transcription factor. Cell 96, 857-868 (Pubitemid 29165088)
43. Kato, M., Yuan, H., Xu, Z. G., Lanting, L., Li, S. L., Wang, M., Hu, M. C., Reddy, M. A., and Natarajan, R. (2006) Role of the Akt/FoxO3a pathway in TGF-β1-mediated mesangial cell dysfunction.Anovel mechanism related to diabetic kidney disease. J. Am. Soc. Nephrol. 17, 3325-3335 (Pubitemid 44865275)
44. Lamouille, S., and Derynck, R. (2007) Cell size and invasion in TGF-β-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J. Cell Biol. 178, 437-451 (Pubitemid 47196152)
45. Rahimi, R. A., Andrianifahanana, M., Wilkes, M. C., Edens, M., Kottom, T. J., Blenis, J., and Leof, E. B. (2009) Distinct roles for mammalian target of rapamycin complexes in the fibroblast response to transforming growth factor-β. Cancer Res. 69, 84-93
46. Magnuson, B., Ekim, B., and Fingar, D. C. (2012) Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem. J. 441, 1-21