A novel regulatory pathway in granulosa cells, the LH/human chorionic gonadotropin-microRNA-125a-3p-Fyn pathway, is required for ovulation

FASEB Journal

Volumn 29, Issue 8, 2015, Pages 3206-3216

  Grossman, Hadas ^a   Chuderland, Dana ^a   Ninio Many, Lihi ^a   Hasky, Noa ^a   Kaplan Kraicer, Ruth ^a   Shalgi, Ruth ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Migration; miRNA; Ovary; Src family kinases

Indexed keywords

CHORIONIC GONADOTROPIN; FOCAL ADHESION KINASE; LUTEINIZING HORMONE; MESSENGER RNA; MICRORNA; MICRORNA 125A; PAXILLIN; PROTEIN KINASE FYN; RECOMBINANT CHORIONIC GONADOTROPIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FOCAL ADHESION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GRANULOSA CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VIVO STUDY; MOUSE; NONHUMAN; OOCYTE; OVULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REPORTER GENE; RNA INTERFERENCE; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL MOTION; GENETICS; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

RATTUS;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CHORIONIC GONADOTROPIN; DOWN-REGULATION; FEMALE; GRANULOSA CELLS; HUMANS; MICE; MICRORNAS; OOCYTES; OVULATION; PROTO-ONCOGENE PROTEINS C-FYN; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84940417307     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-269449     Document Type: Article

References (39)

1. Duggavathi, R., and Murphy, B. D. (2009) Development. Ovulation signals. Science 324, 890-891
2. Inui, M., Martello, G., and Piccolo, S. (2010) MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 252-263
3. Baley, J., and Li, J. (2012) MicroRNAs and ovarian function. J. Ovarian Res. 5, 8
4. Yao,N., Yang,B.Q.,Liu, Y.,Tan,X.Y., Lu,C.L., Yuan,X.H., and Ma, X. (2010) Follicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells. Endocrine 38, 158-166
5. Fiedler, S.D.,Carletti,M. Z.,Hong, X., and Christenson, L.K. (2008) Hormonal regulation of MicroRNA expression in periovulatory mouse mural granulosa cells. Biol. Reprod. 79, 1030-1037
6. Lei, L., Jin, S., Gonzalez, G., Behringer, R. R., and Woodruff, T. K. (2010) The regulatory role of Dicer in folliculogenesis in mice. Mol. Cell. Endocrinol. 315, 63-73
7. Nagaraja, A. K., Andreu-Vieyra, C., Franco, H. L., Ma, L., Chen, R., Han, D. Y., Zhu,H., Agno, J. E., Gunaratne, P.H., DeMayo, F. J., and Matzuk,M.M. (2008)Deletion ofDicer in somatic cells of the female reproductive tract causes sterility. Mol. Endocrinol. 22, 2336-2352
8. Donadeu, F.X., Schauer, S.N., and Sontakke, S. D. (2012) Involvement of miRNAs in ovarian follicular and luteal development. J. Endocrinol. 215, 323-334
9. Sirotkin, A. V., Lauková, M., Ovcharenko, D., Brenaut, P., and Mlyncek,M. (2010) Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J. Cell. Physiol. 223, 49-56
10. Sirotkin, A. V., Ovcharenko, D., Grossmann, R., Lauková, M., and Mlyncek,M. (2009) Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J. Cell. Physiol. 219, 415-420
11. Sang, Q., Yao, Z., Wang, H., Feng, R., Wang, H., Zhao, X., Xing, Q., Jin, L., He, L., Wu, L., and Wang, L. (2013) Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J. Clin. Endocrinol. Metab. 98, 3068-3079
12. Ninio-Many, L., Grossman, H., Shomron, N., Chuderland, D., and Shalgi, R. (2013) microRNA-125a-3p reduces cell proliferation and migration by targeting Fyn. J. Cell Sci. 126, 2867-2876
13. McGinnis, L. K., Carroll, D. J., and Kinsey, W. H. (2011) Protein tyrosine kinase signaling during oocytematuration and fertilization. Mol. Reprod. Dev. 78, 831-845
14. Levi, M., Maro, B., and Shalgi, R. (2010) The involvement of Fyn kinase in resumption of the first meiotic division in mouse oocytes. Cell Cycle 9, 1577-1589
15. Levi, M., Maro, B., and Shalgi, R. (2010) Fyn kinase is involved in cleavage furrow ingression during meiosis and mitosis. Reproduction 140, 827-834
16. Wayne, C. M., Fan, H.-Y., Cheng, X., and Richards, J. S. (2007) Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol. Endocrinol. 21, 1940-1957
17. Saito, Y. D., Jensen, A. R., Salgia, R., and Posadas, E.M. (2010) Fyn: a novel molecular target in cancer. Cancer 116, 1629-1637
18. Mizutani, T., Shiraishi, K., Welsh, T., and Ascoli, M. (2006) Activation of the lutropin/choriogonadotropin receptor in MA-10 cells leads to the tyrosine phosphorylation of the focal adhesion kinase by a pathway that involves Src family kinases.Mol. Endocrinol. 20, 619-630
19. Yeo, M. G.,Oh, H. J.,Cho,H. S., Chun, J. S., Marcantonio, E. E., and Song, W. K. (2011) Phosphorylation of Ser 21 in Fyn regulates its kinase activity, focal adhesion targeting, and is required for cell migration. J. Cell. Physiol. 226, 236-247
20. Rolaki, A., Coukos, G., Loutradis, D., DeLisser, H.M., Coutifaris, C., and Makrigiannakis, A. (2007) Luteogenic hormones act through a vascular endothelial growth factor-dependent mechanism to upregulate alpha 5 beta 1 and alpha v beta 3 integrins, promoting the migration and survival of human luteinized granulosa cells. Am. J. Pathol. 170, 1561-1572
21. Franz,M. B.,Daube, S.,Keck,C., Sator,M., and Pietrowski, D. (2013) SmallGTPases are involved in sprout formation in human granulosa lutein cells. Arch. Gynecol. Obstet. 287, 819-824
22. Cohen-Fredarow, A., Tadmor, A., Raz, T., Meterani, N., Addadi, Y., Nevo, N.,Solomonov, I., Sagi, I.,Mor, G.,Neeman,M., and Dekel, N. (2014) Ovarian dendritic cells act as a double-edged pro-ovulatory and anti-inflammatory sword. Mol. Endocrinol. 28, 1039-1054
23. Roland, A. V., Nunemaker, C. S., Keller, S. R., and Moenter, S. M. (2010) Prenatal androgen exposure programs metabolic dysfunction in female mice. J. Endocrinol. 207, 213-223
24. Suh, B. S., Sprengel, R., Keren-Tal, I., Himmelhoch, S., and Amsterdam, A. (1992) Introduction of a gonadotropin receptor expression plasmid into immortalized granulosa cells leads to reconstitution of hormone-dependent steroidogenesis. J. Cell Biol. 119, 439-450
25. Chuderland, D., Hasky, N., Ben-Ami, I., Kaplan-Kraicer, R., Grossman, H., and Shalgi, R. (2013) A physiological approach for treating endometriosis by recombinant pigment epithelium-derived factor (PEDF). Hum. Reprod. 28, 1626-1634
26. Obernosterer, G., Martinez, J., and Alenius, M. (2007) Locked nucleic acid-based in situ detection of microRNAs in mouse tissue sections. Nat. Protoc. 2, 1508-1514
27. Stocco,C., Telleria, C., and Gibori, G. (2007) Themolecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117-149
28. Jiang, L., Huang, Q., Zhang, S., Zhang, Q., Chang, J., Qiu, X., and Wang, E. (2010) Hsa-miR-125a-3p and hsa-miR-125a-5p are downregulated in non-small cell lung cancer and have inverse effects on invasion and migration of lung cancer cells. BMC Cancer 10, 318
29. Schaller,M.D.,Hildebrand, J. D., and Parsons, J.T. (1999)Complex formation with focal adhesion kinase: A mechanism to regulate activity and subcellular localization of Src kinases. Mol. Biol. Cell 10, 3489-3505
30. Calalb, M. B., Polte, T. R., and Hanks, S. K. (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol. Cell. Biol. 15, 954-963
31. Calalb, M. B., Zhang, X., Polte, T. R., and Hanks, S. K. (1996) Focal adhesion kinase tyrosine-861 is a major site of phosphorylation by Src. Biochem. Biophys. Res. Commun. 228, 662-668
32. Leu, T.-H., and Maa, M.-C. (2002) Tyr-863 phosphorylation enhances focal adhesion kinase autophosphorylation at Tyr-397. Oncogene 21, 6992-7000
33. Mitra, S. K., Hanson, D. A., and Schlaepfer, D. D. (2005) Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68
34. Puttabyatappa,M., Jacot, T. A., Al-Alem, L. F., Rosewell, K. L., Duffy, D. M., Brännström, M., and Curry, Jr., T. E. (2014) Ovarian membrane-type matrix metalloproteinases: induction of MMP14 and MMP16 during the periovulatory period in the rat, macaque, and human. Biol. Reprod. 91, 34
35. Huang, B., Luo, W., Sun, L., Zhang, Q., Jiang, L., Chang, J., Qiu, X., and Wang, E. (2013) MiRNA-125a-3p is a negative regulator of the RhoA-Actomyosin pathway in A549 cells. Int. J. Oncol. 42, 1734-1742
36. Xu, D., Kishi, H., Kawamichi, H., Kajiya, K., Takada, Y., and Kobayashi, S. (2012) Sphingosylphosphorylcholine induces stress fiber formation via activation of Fyn-RhoA-ROCK signaling pathway in fibroblasts. Cell. Signal. 24, 282-289
37. Kawashima, I., Liu, Z.,Mullany, L. K.,Mihara, T., Richards, J. S., and Shimada, M. (2012) EGF-like factors induce expansion of the cumulus cell-oocyte complexes by activating calpain-mediated cell movement. Endocrinology 153, 3949-3959
38. Akison,L.K.,Alvino,E.R.,Dunning,K.R.,Robker,R.L., and Russell, D. L. (2012) Transient invasivemigration in mouse cumulus oocyte complexes induced at ovulationby luteinizinghormone. Biol.Reprod. 86, 125
39. Hess, K. A., Chen, L., and Larsen, W. J. (1999) Inter-Alpha-inhibitor binding to hyaluronan in the cumulus extracellular matrix is required for optimal ovulation and development of mouse oocytes. Biol. Reprod. 61, 436-443