Hes1 in the somatic cells of the murine ovary is necessary for oocyte survival and maturation

Developmental Biology

Volumn 375, Issue 2, 2013, Pages 140-151

  Manosalva, Iris ^a,b   González, Aitor ^a,b,c   Kageyama, Ryoichiro ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Fertility; Hes1; Mouse; Notch pathway; Oocytes; Ovary

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; KI 67 ANTIGEN; MESSENGER RNA; NOTCH RECEPTOR; TRANSCRIPTION FACTOR HES 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL NUCLEUS; CELL PROLIFERATION; CELL SIZE; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FERTILITY; FETUS; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; HES1 GENE; IMMUNOHISTOCHEMISTRY; INHBB GENE; NONHUMAN; OOCYTE MATURATION; OVARY DEVELOPMENT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SOMATIC CELL;

INVERTEBRATA; MAMMALIA; MURINAE;

EID: 84874259602     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.12.015     Document Type: Article

References (45)

1. Andersson E.R., Sandberg R., Lendahl U. Notch signaling: simplicity in design, versatility in function. Development 2011, 138:3593-3612.
2. Dissen G.A., Romero C., Hirshfield A.N., Ojeda S.R. Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 2001, 142:2078-2086.
3. Doneda L., Klinger F.-G., Larizza L., Felici M.D. KL/KIT co-expression in mouse fetal oocytes. Int. J. Dev. Biol. 2002, 46:1015-1021.
4. Driancourt M.A., Reynaud K., Cortvrindt R., Smitz J. Roles of KIT and KIT LIGAND in ovarian function. Rev. Reprod. 2000, 5:143-152.
5. Dykema J.C., Mayo K.E. Two messenger ribonucleic acids encoding the common beta B-chain of inhibin and activin have distinct 5'-initiation sites and are differentially regulated in rat granulosa cells. Endocrinology 1994, 135:702-711.
6. Ghafari F., Gutierrez C.G., Hartshorne G.M. Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one. BMC Dev. Biol. 2007, 7:87.
7. Hahn K.L., Johnson J., Beres B.J., Howard S., Wilson-Rawls J. Lunatic fringe null female mice are infertile due to defects in meiotic maturation. Development 2005, 132:817-828.
8. Han H., Tanigaki K., Yamamoto N., Kuroda K., Yoshimoto M., Nakahata T., Ikuta K., Honjo T. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 2002, 14:637-645.
9. Hopfer O., Zwahlen D., Fey M.F., Aebi S. The Notch pathway in ovarian carcinomas and adenomas. Br. J. Cancer 2005, 93:709-718.
10. Imayoshi I., Sakamoto M., Yamaguchi M., Mori K., Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 2010, 30:3489-3498.
11. Imayoshi I., Shimogori T., Ohtsuka T., Kageyama R. Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 2008, 135:2531-2541.
12. Ishibashi M., Ang S.L., Shiota K., Nakanishi S., Kageyama R., Guillemot F. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 1995, 9:3136-3148.
13. Jamin S.P., Arango N.A., Mishina Y., Hanks M.C., Behringer R.R. Requirement of Bmpr1a for Müllerian duct regression during male sexual development. Nat. Genet. 2002, 32:408-410.
14. Jin X., Han C.-S., Yu F.-Q., Wei P., Hu Z.-Y., Liu Y.-X. Anti-apoptotic action of stem cell factor on oocytes in primordial follicles and its signal transduction. Mol. Reprod. Dev. 2005, 70:82-90.
15. John G.B., Shidler M.J., Besmer P., Castrillon D.H. Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev. Biol. 2009, 331:292-299.
16. Johnson J., Espinoza T., McGaughey R.W., Rawls A., Wilson-Rawls J. Notch pathway genes are expressed in mammalian ovarian follicles. Mech. Dev. 2001, 109:355-361.
17. Kageyama R., Ohtsuka T., Kobayashi T. The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 2007, 134:1243-1251.
18. Kageyama R., Ohtsuka T., Shimojo H., Imayoshi I. Dynamic Notch signaling in neural progenitor cells and a revised view of lateral inhibition. Nat. Neurosci. 2008, 11:1247-1251.
19. Klusza S., Deng W.-M. At the crossroads of differentiation and proliferation: precise control of cell-cycle changes by multiple signaling pathways in Drosophila follicle cells. Bioessays 2011, 33:124-134.
20. Kobayashi T., Mizuno H., Imayoshi I., Furusawa C., Shirahige K., Kageyama R. The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 2009, 23:1870-1875.
21. Liu C.-F., Parker K., Yao H.H.-C. WNT4/beta-catenin pathway maintains female germ cell survival by inhibiting activin beta B in the mouse fetal ovary. PLoS One 2010, 5:e10382.
22. Lomelí H., Ramos-Mejía V., Gertsenstein M., Lobe C.G., Nagy A. Targeted insertion of Cre recombinase into the TNAP gene: excision in primordial germ cells. Genesis 2000, 26:116-117.
23. Masamizu Y., Ohtsuka T., Takashima Y., Nagahara H., Takenaka Y., Yoshikawa K., Okamura H., Kageyama R. Real-time imaging of the somite segmentation clock: revelation of unstable oscillators in the individual presomitic mesoderm cells. Proc. Natl. Acad. Sci. USA 2006, 103:1313-1318.
24. Mazaud S., Oréal E., Guigon C.J., Carré-Eusèbe D., Magre S. Lhx9 expression during gonadal morphogenesis as related to the state of cell differentiation. Gene Expr. Patterns 2002, 2:373-377.
25. Murtaugh L.C., Stanger B.Z., Kwan K.M., Melton D.A. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 2003, 100:14920-14925.
26. Ottolenghi C., Pelosi E., Tran J., Colombino M., Douglass E., Nedorezov T., Cao A., Forabosco A., Schlessinger D. Loss of Wnt4 and Foxl2 leads to female-to-male sex reversal extending to germ cells. Hum. Mol. Genet. 2007, 16:2795-2804.
27. Packer A.I., Hsu Y.C., Besmer P., Bachvarova R.F. The ligand of the c-kit receptor promotes oocyte growth. Dev. Biol. 1994, 161:194-205.
28. Parrott J.A., Skinner M.K. Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology 1999, 140:4262-4271.
29. Pepling M.E., Spradling A.C. Female mouse germ cells form synchronously dividing cysts. Development 1998, 125:3323-3328.
30. Phillips D.J., de Kretser D.M. Follistatin: a multifunctional regulatory protein. Front. Neuroendocrinol. 1998, 19:287-322.
31. Rajareddy S., Reddy P., Du C., Liu L., Jagarlamudi K., Tang W., Shen Y., Berthet C., Peng S.L., Kaldis P., Liu K. p27kip1 (Cyclin-dependent kinase inhibitor 1B) controls ovarian development by suppressing follicle endowment and activation and promoting follicle atresia in mice. Mol. Endocrinol. 2007, 21:2189-2202.
32. Ratts V.S., Flaws J.A., Kolp R., Sorenson C.M., Tilly J.L. Ablation of bcl-2 gene expression decreases the numbers of oocytes and primordial follicles established in the post-natal female mouse gonad. Endocrinology 1995, 136:3665-3668.
33. Reynaud K., Cortvrindt R., Smitz J., Driancourt M.A. Effects of Kit Ligand and anti-Kit antibody on growth of cultured mouse preantral follicles. Mol. Reprod. Dev. 2000, 56:483-494.
34. Shimojo H., Ohtsuka T., Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008, 58:52-64.
35. Speed R.M. Meiosis in the foetal mouse ovary. I. An analysis at the light microscope level using surface-spreading. Chromosoma 1982, 85:427-437.
36. Tateya T., Imayoshi I., Tateya I., Ito J., Kageyama R. Cooperative functions of Hes/Hey genes in auditory hair cell and supporting cell development. Dev. Biol. 2011, 352:329-340.
37. Tang H., Brennan J., Karl J., Hamada Y., Raetzman L., Capel B. Notch signaling maintains Leydig progenitor cells in the mouse testis. Development 2008, 135:3745-3753.
38. Trombly D.J., Woodruff T.K., Mayo K.E. Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 2009, 150:1014-1024.
39. Uda M., Ottolenghi C., Crisponi L., Garcia J.E., Deiana M., Kimber W., Forabosco A., Cao A., Schlessinger D., Pilia G. Foxl2 disruption causes mouse ovarian failure by pervasive blockage of follicle development. Hum. Mol. Genet. 2004, 13:1171-1181.
40. Ueo T., Imayoshi I., Kobayashi T., Ohtsuka T., Seno H., Nakase H., Chiba T., Kageyama R. The role of Hes genes in intestinal development, homeostasis and tumor formation. Development 2012, 139:1071-1082.
41. Veitia R.A. FOXL2 versus SOX9: a lifelong battle of the sexes. Bioessays 2010, 32:375-380.
42. Wang M., Wu L., Wang L., Xin X. Down-regulation of Notch1 by gamma-secretase inhibition contributes to cell growth inhibition and apoptosis in ovarian cancer cells A2780. Biochem. Biophys. Res. Commun. 2010, 393:144-149.
43. Waters K.A., Reinke V. Extrinsic and intrinsic control of germ cell proliferation in Caenorhabditis elegans. Mol. Reprod. Dev. 2011, 78:151-160.
44. Yao H.H.C., Matzuk M.M., Jorgez C.J., Menke D.B., Page D.C., Swain A., Capel B. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev. Dyn. 2004, 230:210-215.
45. Yao H.H.-C., Aardema J., Holthusen K. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol. Reprod. 2006, 74:978-983.