35
Views
46
CrossRef citations to date
0
Altmetric
Article

FIGLA, a Basic Helix-Loop-Helix Transcription Factor, Balances Sexually Dimorphic Gene Expression in Postnatal Oocytes

, , , &
Pages 3661-3671 | Received 18 Feb 2010, Accepted 06 May 2010, Published online: 20 Mar 2023

REFERENCES

  • Adham, I. M., K. Nayernia, E. Burkhardt-Gottges, O. Topaloglu, C. Dixkens, A. F. Holstein, and W. Engel. 2001. Teratozoospermia in mice lacking the transition protein 2 (Tnp2). Mol. Hum. Reprod. 7:513–520.
  • Alban, A., S. O. David, L. Bjorkesten, C. Andersson, E. Sloge, S. Lewis, and I. Currie. 2003. A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3:36–44.
  • Ballow, D., M. L. Meistrich, M. Matzuk, and A. Rajkovic. 2006. Sohlh1 is essential for spermatogonial differentiation. Dev. Biol. 294:161–167.
  • Barrera, L. O. 2006. The transcriptional regulatory code of eukaryotic cells: insights from genome-wide analysis of chromatin organization and transcription factor binding. Curr. Opin. Cell Biol. 18:291–298.
  • Brennan, J., and B. Capel. 2004. One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat. Rev. Genet. 5:509–521.
  • Buaas, F. W., A. L. Kirsh, M. Sharma, D. J. McLean, J. L. Morris, M. D. Griswold, D. G. de Rooij, and R. E. Braun. 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36:647–652.
  • Burgoyne, P. S., S. K. Mahadevaiah, and J. M. Turner. 2009. The consequences of asynapsis for mammalian meiosis. Nat. Rev. Genet. 10:207–216.
  • Cho, C., H. Jung-Ha, W. D. Willis, E. H. Goulding, P. Stein, Z. Xu, R. M. Schultz, N. B. Hecht, and E. M. Eddy. 2003. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol. Reprod. 69:211–217.
  • Cho, C., W. D. Willis, E. H. Goulding, H. Jung-Ha, Y. C. Choi, N. B. Hecht, and E. M. Eddy. 2001. Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat. Genet. 28:82–86.
  • Chuma, S., M. Hosokawa, K. Kitamura, S. Kasai, M. Fujioka, M. Hiyoshi, K. Takamune, T. Noce, and N. Nakatsuji. 2006. Tdrd1/Mtr-1, a tudor-related gene, is essential for male germ-cell differentiation and nuage/germinal granule formation in mice. Proc. Natl. Acad. Sci. U. S. A. 103:15894–15899.
  • Connolly, C. M., A. T. Dearth, and R. E. Braun. 2005. Disruption of murine Tenr results in teratospermia and male infertility. Dev. Biol. 278:13–21.
  • Eddy, E. M. 1975. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43:229–280.
  • Fawcett, D. W., E. M. Eddy, and D. M. Phillips. 1970. Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol. Reprod. 2:129–153.
  • Fulco, M., R. L. Schiltz, S. Iezzi, M. T. King, P. Zhao, Y. Kashiwaya, E. Hoffman, R. L. Veech, and V. Sartorelli. 2003. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol. Cell 12:51–62.
  • Ganguly, A., R. A. McKnight, S. Raychaudhuri, B. C. Shin, Z. Ma, K. Moley, and S. U. Devaskar. 2007. Glucose transporter isoform-3 mutations cause early pregnancy loss and fetal growth restriction. Am. J. Physiol. Endocrinol. Metab. 292:E1241–E1255.
  • Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493–501.
  • Hoodbhoy, T., S. Joshi, E. S. Boja, S. A. Williams, P. Stanley, and J. Dean. 2005. Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J. Biol. Chem. 280:12721–12731.
  • Hosokawa, M., M. Shoji, K. Kitamura, T. Tanaka, T. Noce, S. Chuma, and N. Nakatsuji. 2007. Tudor-related proteins TDRD1/MTR-1, TDRD6 and TDRD7/TRAP: domain composition, intracellular localization, and function in male germ cells in mice. Dev. Biol. 301:38–52.
  • Jones, S. 2004. An overview of the basic helix-loop-helix proteins. Genome Biol. 5:226.
  • Joshi, S., H. Davies, L. P. Sims, S. E. Levy, and J. Dean. 2007. Ovarian gene expression in the absence of FIGLA, an oocyte-specific transcription factor. BMC Dev. Biol. 7:67.
  • Kai, T., and A. Spradling. 2004. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428:564–569.
  • Kido, T., and Y. F. Lau. 2005. A Cre gene directed by a human TSPY promoter is specific for germ cells and neurons. Genesis 42:263–275.
  • Kotaja, N., and P. Sassone-Corsi. 2007. The chromatoid body: a germ-cell-specific RNA-processing centre. Nat. Rev. Mol. Cell Biol. 8:85–90.
  • Kuramochi-Miyagawa, S., T. Kimura, T. W. Ijiri, T. Isobe, N. Asada, Y. Fujita, M. Ikawa, N. Iwai, M. Okabe, W. Deng, H. Lin, Y. Matsuda, and T. Nakano. 2004. Mili, a mammalian member of Piwi family gene, is essential for spermatogenesis. Development 131:839–849.
  • La Salle, S., F. Sun, X. D. Zhang, M. J. Matunis, and M. A. Handel. 2008. Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev. Biol. 321:227–237.
  • Leduc, F., V. Maquennehan, G. B. Nkoma, and G. Boissonneault. 2008. DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol. Reprod. 78:324–332.
  • Li, L., B. Baibakov, and J. Dean. 2008. A subcortical maternal complex essential for pre-implantation mouse embryogenesis. Dev. Cell 15:416–425.
  • Liang, L.-F., S. M. Soyal, and J. Dean. 1997. FIGα, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 124:4939–4949.
  • Liu, Y., Z. X. Yao, C. Bendavid, C. Borgmeyer, Z. Han, L. R. Cavalli, W. Y. Chan, J. Folmer, B. R. Zirkin, B. R. Haddad, G. I. Gallicano, and V. Papadopoulos. 2005. Haploinsufficiency of cytochrome P450 17α-hydroxylase/17,20 lyase (CYP17) causes infertility in male mice. Mol. Endocrinol. 19:2380–2389.
  • Lu, J., R. Webb, J. A. Richardson, and E. N. Olson. 1999. MyoR: a muscle-restricted basic helix-loop-helix transcription factor that antagonizes the actions of MyoD. Proc. Natl. Acad. Sci. U. S. A. 96:552–557.
  • Mal, A., M. Sturniolo, R. L. Schiltz, M. K. Ghosh, and M. L. Harter. 2001. A role for histone deacetylase HDAC1 in modulating the transcriptional activity of MyoD: inhibition of the myogenic program. EMBO J. 20:1739–1753.
  • Newman, G. R. 1999. LR White embedding for immunoelectron microscopy. Histochem. J. 31:79.
  • Otori, M., T. Karashima, and M. Yamamoto. 2006. The Caenorhabditis elegans homologue of deleted in azoospermia is involved in the sperm/oocyte switch. Mol. Biol. Cell 17:3147–3155.
  • Pan, J., S. Eckardt, N. A. Leu, M. G. Buffone, J. Zhou, G. L. Gerton, K. J. McLaughlin, and P. J. Wang. 2009. Inactivation of Nxf2 causes defects in male meiosis and age-dependent depletion of spermatogonia. Dev. Biol. 330:167–174.
  • Pfeifer, C., P. D. Thomsen, and H. Scherthan. 2001. Centromere and telomere redistribution precedes homologue pairing and terminal synapsis initiation during prophase I of cattle spermatogenesis. Cytogenet. Cell Genet. 93:304–314.
  • Rajkovic, A., S. A. Pangas, D. Ballow, N. Suzumori, and M. M. Matzuk. 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305:1157–1159.
  • Rankin, T., P. Talbot, E. Lee, and J. Dean. 1999. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development 126:3847–3855.
  • Rankin, T. L., Z.-B. Tong, P. E. Castle, E. Lee, R. Gore-Langton, L. M. Nelson, and J. Dean. 1998. Human ZP3 restores fertility in Zp3 null mice without affecting order-specific sperm binding. Development 125:2415–2424.
  • Ravnik, S. E., and D. J. Wolgemuth. 1999. Regulation of meiosis during mammalian spermatogenesis: the A-type cyclins and their associated cyclin-dependent kinases are differentially expressed in the germ-cell lineage. Dev. Biol. 207:408–418.
  • Remenyi, A., H. R. Scholer, and M. Wilmanns. 2004. Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11:812–815.
  • Reuter, M., S. Chuma, T. Tanaka, T. Franz, A. Stark, and R. S. Pillai. 2009. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat. Struct. Mol. Biol. 16:639–646.
  • Sada, A., A. Suzuki, H. Suzuki, and Y. Saga. 2009. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325:1394–1398.
  • Sartorelli, V., P. L. Puri, Y. Hamamori, V. Ogryzko, G. Chung, Y. Nakatani, J. Y. Wang, and L. Kedes. 1999. Acetylation of MyoD directed by PCAF is necessary for the execution of the muscle program. Mol. Cell 4:725–734.
  • Schubert, S., B. Skawran, F. Dechend, K. Nayernia, A. Meinhardt, I. Nanda, M. Schmid, W. Engel, and J. Schmidtke. 2003. Generation and characterization of a transgenic mouse with a functional human TSPY. Biol. Reprod. 69:968–975.
  • Simone, C., S. V. Forcales, D. A. Hill, A. N. Imbalzano, L. Latella, and P. L. Puri. 2004. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat. Genet. 36:738–743.
  • Soyal, S. M., A. Amleh, and J. Dean. 2000. FIGα, a germ-cell specific transcription factor required for ovarian follicle formation. Development 127:4645–4654.
  • Suzuki, A., and Y. Saga. 2008. Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev. 22:430–435.
  • Tanaka, S. S., Y. Toyooka, R. Akasu, Y. Katoh-Fukui, Y. Nakahara, R. Suzuki, M. Yokoyama, and T. Noce. 2000. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev. 14:841–853.
  • Tapscott, S. J. 2005. The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132:2685–2695.
  • Tsuda, M., Y. Sasaoka, M. Kiso, K. Abe, S. Haraguchi, S. Kobayashi, and Y. Saga. 2003. Conserved role of nanos proteins in germ cell development. Science 301:1239–1241.
  • Uhlenhaut, N. H., S. Jakob, K. Anlag, T. Eisenberger, R. Sekido, J. Kress, A. C. Treier, C. Klugmann, C. Klasen, N. I. Holter, D. Riethmacher, G. Schutz, A. J. Cooney, R. Lovell-Badge, and M. Treier. 2009. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130–1142.
  • Vasileva, A., D. Tiedau, A. Firooznia, T. Muller-Reichert, and R. Jessberger. 2009. Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr. Biol. 19:630–639.
  • Wang, J., J. P. Saxe, T. Tanaka, S. Chuma, and H. Lin. 2009. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr. Biol. 19:640–644.
  • Yan, W., L. Ma, K. H. Burns, and M. M. Matzuk. 2004. Haploinsufficiency of kelch-like protein homolog 10 causes infertility in male mice. Proc. Natl. Acad. Sci. U. S. A. 101:7793–7798.
  • Yeung, C. H., A. Wagenfeld, E. Nieschlag, and T. G. Cooper. 2000. The cause of infertility of male c-ros tyrosine kinase receptor knockout mice. Biol. Reprod. 63:612–618.
  • Yokota, S. 2008. Historical survey on chromatoid body research. Acta Histochem. Cytochem. 41:65–82.
  • Zhao, M., C. R. Shirley, Y. E. Yu, B. Mohapatra, Y. Zhang, E. Unni, J. M. Deng, N. A. Arango, N. H. Terry, M. M. Weil, L. D. Russell, R. R. Behringer, and M. L. Meistrich. 2001. Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol. Cell. Biol. 21:7243–7255.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.