New Understandings on Folliculogenesis/Oogenesis Regulation in Mouse as Revealed by Conditional Knockout

Journal of Genetics and Genomics

Volumn 39, Issue 2, 2012, Pages 61-68

  Hu, M W ^a,b   Wang, Z B ^a   Schatten, H ^c   Sun, Qing Yuan ^a  

^a INSTITUTE OF ZOOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF MISSOURI   (United States)

Author keywords

Conditional knockout; Folliculogenesis; Mouse; Oogenesis

Indexed keywords

ANDROGEN RECEPTOR; BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR GATA 4; WNT4 PROTEIN;

CELL DIFFERENTIATION; CELL PROLIFERATION; GENE DELETION; GENE FUNCTION; LUTEINIZATION; MEIOSIS; MITOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PROMETAPHASE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; FEMALE; MICE; MICE, KNOCKOUT; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; SIGNAL TRANSDUCTION;

EID: 84862824382     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2012.01.004     Document Type: Review

References (52)

1. Adhikari D., Flohr G., Gorre N., Shen Y., Yang H., Lundin E., Lan Z., Gambello M.J., Liu K. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol. Hum. Reprod. 2009, 15:765-770.
2. Adhikari D., Zheng W., Shen Y., Gorre N., Hämäläinen T., Cooney A.J., Huhtaniemi I., Lan Z.-J., Liu K. Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum. Mol. Genet. 2010, 19:397-410.
3. Alfieri J.A., Martin A.D., Takeda J., Kondoh G., Myles D.G., Primakoff P. Infertility in female mice with an oocyte-specific knockout of GPI-anchored proteins. J. Cell Sci. 2003, 116:2149-2155.
4. Andreu-Vieyra C.V., Chen R., Agno J.E., Glaser S., Anastassiadis K., Stewart A.F., Matzuk M.M. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 2010, 8:e1000453.
5. Arango N.A., Kobayashi A., Wang Y., Jamin S.P., Lee H.-H., Orvis G.D., Behringer R.R. A mesenchymal perspective of Müllerian duct differentiation and regression in Amhr2-lacZ mice. Mol. Reprod. Dev. 2008, 75:1154-1162.
6. Audouard C., Le Masson F., Charry C., Li Z., Christians E.S. Oocyte-targeted deletion reveals that hsp90b1 is needed for the completion of first mitosis in mouse zygotes. PLoS ONE 2011, 6:e17109.
7. Boyer A., Lapointe E., Zheng X., Cowan R.G., Li H., Quirk S.M., DeMayo F.J., Richards J.S., Boerboom D. WNT4 is required for normal ovarian follicle development and female fertility. FASEB J. 2010, 24:3010-3025.
8. Choi M., Lee O.-H., Jeon S., Park M., Lee D.R., Ko J.-J., Yoon T.K., Rajkovic A., Choi Y. The oocyte-specific transcription factor, Nobox, regulates the expression of Pad6, a peptidylarginine deiminase in the oocyte. FEBS Lett. 2010, 584:3629-3634.
9. Choi Y., Yuan D., Rajkovic A. Germ cell-specific transcriptional regulator sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol. Reprod. 2008, 79:1176-1182.
10. Edson M.A., Nalam R.L., Clementi C., Franco H.L., DeMayo F.J., Lyons K.M., Pangas S.A., Matzuk M.M. Granulosa cell-expressed BMPR1A and BMPR1B have unique functions in regulating fertility but act redundantly to suppress ovarian tumor development. Mol. Endocrinol. 2010, 24:1251-1266.
11. Fan H.-Y., Richards J.S. Minireview: physiological and pathological actions of RAS in the ovary. Mol. Endocrinol. 2010, 24:286-298.
12. Fan H.-Y., Liu Z., Cahill N., Richards J.S. Targeted disruption of Pten in ovarian granulosa cells enhances ovulation and extends the life span of luteal cells. Mol. Endocrinol. 2008, 22:2128-2140.
13. Fan H.-Y., Liu Z., Johnson P.F., Richards J.S. CCAAT/enhancer-binding proteins (C/EBP)-α and -β are essential for ovulation, luteinization, and the expression of key target genes. Mol. Endocrinol. 2011, 25:253-268.
14. Fan H.-Y., O'Connor A., Shitanaka M., Shimada M., Liu Z., Richards J.S. β-catenin (CTNNB1) promotes preovulatory follicular development but represses LH-mediated ovulation and luteinization. Mol. Endocrinol. 2010, 24:1529-1542.
15. Fan H.-Y., Liu Z., Shimada M., Sterneck E., Johnson P.F., Hedrick S.M., Richards J.S. MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 2009, 324:938-941.
16. G12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development 2008, 135:2127-2137.
17. Gama Sosa M.A., De Gasperi R., Elder G.A. Animal transgenesis: an overview. Brain Struct. Funct. 2010, 214:91-109.
18. Gershon E., Plaks V., Aharon I., Galiani D., Reizel Y., Sela-Abramovich S., Granot I., Winterhager E., Dekel N. Oocyte-directed depletion of connexin43 using the Cre-LoxP system leads to subfertility in female mice. Dev. Biol. 2008, 313:1-12.
19. Griffith G.J., Trask M.C., Hiller J., Walentuk M., Pawlak J.B., Tremblay K.D., Mager J. Yin-yang1 is required in the mammalian oocyte for follicle expansion. Biol. Reprod. 2011, 84:654-663.
20. Hached K., Xie S.Z., Buffin E., Cladiere D., Rachez C., Sacras M., Sorger P.K., Wassmann K. Mps1 at kinetochores is essential for female mouse meiosis I. Development 2011, 138:2261-2271.
21. Hammond S.S., Matin A. Tools for the genetic analysis of germ cells. Genesis 2009, 47:617-627.
22. Hernandez Gifford J.A., Hunzicker-Dunn M.E., Nilson J.H. Conditional deletion of β-catenin mediated by Amhr2cre in mice causes female infertility. Biol. Reprod. 2009, 80:1282-1292.
23. Hsieh M., Thao K., Conti M. Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLoS ONE 2011, 6:e21574.
24. Jagarlamudi K., Liu L., Adhikari D., Reddy P., Idahl A., Ottander U., Lundin E., Liu K. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS ONE 2009, 4:e6186.
25. John G.B., Gallardo T.D., Shirley L.J., Castrillon D.H. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev. Biol. 2008, 321:197-204.
26. Kaneda M., Hirasawa R., Chiba H., Okano M., Li E., Sasaki H. Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 2010, 15:169-179.
27. Kudo N.R., Wassmann K., Anger M., Schuh M., Wirth K.G., Xu H., Helmhart W., Kudo H., McKay M., Maro B., Ellenberg J., de Boer P., Nasmyth K. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 2006, 126:135-146.
28. Kyrönlahti A., Vetter M., Euler R., Bielinska M., Jay P.Y., Anttonen M., Heikinheimo M., Wilson D.B. GATA4 deficiency impairs ovarian function in adult mice. Biol. Reprod. 2011, 84:1033-1044.
29. Lan Z.-J., Xu X., Cooney A.J. Differential oocyte-specific expression of Cre recombinase activity in GDF-9-iCre, Zp3cre, and Msx2Cre transgenic mice. Biol. Reprod. 2004, 71:1469-1474.
30. Lan Z.-J., Gu P., Xu X., Jackson K.J., DeMayo F.J., O'Malley B.W., Cooney A.J. GCNF-dependent repression of BMP-15 and GDF-9 mediates gamete regulation of female fertility. EMBO J. 2003, 22:4070-4081.
31. Lee S., Kang D.-W., Hudgins-Spivey S., Krust A., Lee E.-Y., Koo Y., Cheon Y., Gye M.C., Chambon P., Ko C. Theca-specific estrogen receptor-alpha knockout mice lose fertility prematurely. Endocrinology 2009, 150:3855-3862.
32. Lei L., Jin S., Gonzalez G., Behringer R.R., Woodruff T.K. The regulatory role of Dicer in folliculogenesis in mice. Mol. Cell. Endocrinol. 2010, 315:63-73.
33. Liu Z., Fan H.-Y., Wang Y., Richards J.S. Targeted disruption of Mapk14 (p38MAPKalpha) in granulosa cells and cumulus cells causes cell-specific changes in gene expression profiles that rescue COC expansion and maintain fertility. Mol. Endocrinol. 2010, 24:1794-1804.
34. Matthaei K.I. Genetically manipulated mice: a powerful tool with unsuspected caveats. J. Physiol. 2007, 582.2:481-488.
35. McGuinness B.E., Anger M., Kouznetsova A., Gil-Bernabé A.M., Helmhart W., Kudo N.R., Wuensche A., Taylor S., Hoog C., Novak B., Nasmyth K. Regulation of APC/C activity in oocytes by a Bub1-dependent spindle assembly checkpoint. Curr. Biol. 2009, 19:369-380.
36. Molyneaux K.A., Schaible K., Wylie C. GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation. Development 2003, 130:4287-4294.
37. Nasmyth K., Haering C.H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 2009, 43:525-558.
38. Pangas S.A., Li X., Robertson E.J., Matzuk M.M. Premature luteinization and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol. Endocrinol. 2006, 20:1406-1422.
39. Pitetti J.L., Torre D., Conne B., Papaioannou M.D., Cederroth C.R., Xuan S., Kahn R., Parada L.F., Vassalli J.D., Efstratiadis A., Nef S. Insulin receptor and IGF1R are not required for oocyte growth, differentiation, and maturation in mice. Sex. Dev. 2009, 3:264-272.
40. Reddy P., Adhikari D., Zheng W., Liang S., Hämäläinen T., Tohonen V., Ogawa W., Noda T., Volarevic S., Huhtaniemi I., Liu K. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum. Mol. Genet. 2009, 18:2813-2824.
41. 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., Liu K. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008, 319:611-613.
42. Ren Y., Cowan R.G., Harman R.M., Quirk S.M. Dominant activation of the hedgehog signaling pathway in the ovary alters theca development and prevents ovulation. Mol. Endocrinol. 2009, 23:711-723.
43. Revenkova E., Herrmann K., Adelfalk C., Jessberger R. Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr. Biol. 2010, 20:1-5.
44. Sen A., Hammes S.R. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol. Endocrinol. 2010, 24:1393-1403.
45. Shi S., Williams S.A., Seppo A., Kurniawan H., Chen W., Ye Z., Marth J.D., Stanley P. Inactivation of the Mgat1 gene in oocytes impairs oogenesis, but embryos lacking complex and hybrid N-glycans develop and implant. Mol. Cell. Biol. 2004, 24:9920-9929.
46. Sun Q.-Y., Liu K., Kikuchi K. Oocyte-specific knockout: a novel in vivo approach for studying gene functions during folliculogenesis, oocyte maturation, fertilization, and embryogenesis. Biol. Reprod. 2008, 79:1014-1020.
47. Williams S.A., Stanley P. Mouse fertility is enhanced by oocyte-specific loss of core 1-derived O-glycans. FASEB J. 2008, 22:2273-2284.
48. Williams S.A., Stanley P. Oocyte-specific deletion of complex and hybrid N-glycans leads to defects in preovulatory follicle and cumulus mass development. Reproduction 2009, 137:321-331.
49. Williams S.A., Stanley P. Premature ovarian failure in mice with oocytes lacking core 1-derived O-glycans and complex N-glycans. Endocrinology 2011, 152:1057-1066.
50. Williams S.A., Stanley P. Roles for N- and O-glycans in early mouse development. Adv. Exp. Med. Biol. 2011, 705:397-410.
51. Xu X.D., Fu X.D. Conditional knockout mice to study alternative splicing in vivo. Methods 2005, 37:387-392.
52. Zheng W., Nagaraju G., Liu Z., Liu K. Functional roles of the phosphatidylinositol 3-kinases (PI3Ks) signaling in the mammalian ovary. Mol. Cell. Endocrinol 2011, 2011 June 13 [Epub ahead of print].