Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 29 August 2003:
Vol. 301. no. 5637, pp. 1239 - 1241
DOI: 10.1126/science.1085222

Reports

Conserved Role of nanos Proteins in Germ Cell Development

Masayuki Tsuda,1,2* Yumiko Sasaoka,1* Makoto Kiso,1 Kuniya Abe,3 Seiki Haraguchi,4 Satoru Kobayashi,2,5 Yumiko Saga1,2{dagger}

In Drosophila, maternally supplied Nanos functions in the migration of primordial germ cells (PGCs) into the gonad; in mice, zygotic genes are involved instead. We report the cloning and the functional analyses of nanos2 and nanos3 in mice. These genes are differentially expressed in mouse PGCs. nanos2 is predominantly expressed in male germ cells, and the elimination of this gene results in a complete loss of spermatogonia. However, nanos3 is found in migrating PGCs, and the elimination of this factor results in the complete loss of germ cells in both sexes. Hence, although mice and flies differ in their mechanisms for germ cell specification, there seems to be conserved function for nanos proteins among invertebrates and vertebrates.

1 Division of Mammalian Development, National Institute of Genetics, SOKENDAI, Yata 1111, Mishima, Shizuoka 411-8540, Japan. 2 Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, 2-6-15, Shibakoen, Minato-ku, Tokyo 105-0011, Japan. 3 RIKEN, Bio-Resource Center, 3-1-1 Koyadai, Tsukuba-shi, Ibaraki 305-0074, Japan. 4 Department of Microbiology, Shiga University of Medical Science, Seta, Otsu-shi, Shiga 520-2192, Japan. 5 Center for Integrative Bioscience, National Institute for Basic Biology, Okazaki National Research Institute, Nishigonaka, Myodaiji, Okazaki 444-8585, Japan.



* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: ysaga{at}lab.nig.ac.jp

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells.
S. Yamaguchi, K. Kurimoto, Y. Yabuta, H. Sasaki, N. Nakatsuji, M. Saitou, and T. Tada (2009)
Development 136, 4011-4020
   Abstract »    Full Text »    PDF »
The Mammalian Ovary from Genesis to Revelation.
M. A. Edson, A. K. Nagaraja, and M. M. Matzuk (2009)
Endocr. Rev. 30, 624-712
   Abstract »    Full Text »    PDF »
The RNA-Binding Protein NANOS2 Is Required to Maintain Murine Spermatogonial Stem Cells.
A. Sada, A. Suzuki, H. Suzuki, and Y. Saga (2009)
Science 325, 1394-1398
   Abstract »    Full Text »    PDF »
eIF4A controls germline stem cell self-renewal by directly inhibiting BAM function in the Drosophila ovary.
R. Shen, C. Weng, J. Yu, and T. Xie (2009)
PNAS 106, 11623-11628
   Abstract »    Full Text »    PDF »
Instructing an Embryonic Stem Cell-Derived Oocyte Fate: Lessons from Endogenous Oogenesis.
C. R. Nicholas, S. L. Chavez, V. L. Baker, and R. A. Reijo Pera (2009)
Endocr. Rev. 30, 264-283
   Abstract »    Full Text »    PDF »
Germ cell sex determination in mammals.
A. Kocer, J. Reichmann, D. Best, and I. R. Adams (2009)
Mol. Hum. Reprod. 15, 205-213
   Abstract »    Full Text »    PDF »
The highly conserved NANOS2 protein: testis-specific expression and significance for the human male reproduction.
K.M. Kusz, L. Tomczyk, M. Sajek, A. Spik, A. Latos-Bielenska, P. Jedrzejczak, L. Pawelczyk, and J. Jaruzelska (2009)
Mol. Hum. Reprod. 15, 165-171
   Abstract »    Full Text »    PDF »
Stem Cells Use Distinct Self-renewal Programs at Different Ages.
B.P. Levi and S.J. Morrison (2009)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Less is more: specification of the germline by transcriptional repression.
A. Nakamura and G. Seydoux (2008)
Development 135, 3817-3827
   Abstract »    Full Text »    PDF »
Germ Cell Specification and Regeneration in Planarians.
P.A. Newmark, Y. Wang, and T. Chong (2008)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
A comprehensive, non-invasive visualization of primordial germ cell development in mice by the Prdm1-mVenus and Dppa3-ECFP double transgenic reporter.
Y. Ohinata, M. Sano, M. Shigeta, K. Yamanaka, and M. Saitou (2008)
Reproduction 136, 503-514
   Abstract »    Full Text »    PDF »
Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice.
K. Kurimoto, Y. Yabuta, Y. Ohinata, M. Shigeta, K. Yamanaka, and M. Saitou (2008)
Genes & Dev. 22, 1617-1635
   Abstract »    Full Text »    PDF »
Multiple maternal proteins coordinate to restrict the translation of C. elegans nanos-2 to primordial germ cells.
S. Jadhav, M. Rana, and K. Subramaniam (2008)
Development 135, 1803-1812
   Abstract »    Full Text »    PDF »
In utero exposure to low doses of environmental pollutants disrupts fetal ovarian development in sheep.
P. A. Fowler, N. J. Dora, H. McFerran, M. R. Amezaga, D. W. Miller, R. G. Lea, P. Cash, A. S. McNeilly, N. P. Evans, C. Cotinot, et al. (2008)
Mol. Hum. Reprod. 14, 269-280
   Abstract »    Full Text »    PDF »
Identification and characterization of novel mammalian spermatogenic genes conserved from fly to human.
E. Bonilla and E. Y. Xu (2008)
Mol. Hum. Reprod. 14, 137-142
   Abstract »    Full Text »    PDF »
Nanos2 suppresses meiosis and promotes male germ cell differentiation.
A. Suzuki and Y. Saga (2008)
Genes & Dev. 22, 430-435
   Abstract »    Full Text »    PDF »
The Molecular Chaperone Hsp90 Is Required for mRNA Localization in Drosophila melanogaster Embryos.
Y. Song, L. Fee, T. H. Lee, and R. P. Wharton (2007)
Genetics 176, 2213-2222
   Abstract »    Full Text »    PDF »
Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice.
Y. Seki, M. Yamaji, Y. Yabuta, M. Sano, M. Shigeta, Y. Matsui, Y. Saga, M. Tachibana, Y. Shinkai, and M. Saitou (2007)
Development 134, 2627-2638
   Abstract »    Full Text »    PDF »
Maternal Nanos represses hid/skl-dependent apoptosis to maintain the germ line in Drosophila embryos.
K. Sato, Y. Hayashi, Y. Ninomiya, S. Shigenobu, K. Arita, M. Mukai, and S. Kobayashi (2007)
PNAS 104, 7455-7460
   Abstract »    Full Text »    PDF »
Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline.
L. Y. Kadyrova, Y. Habara, T. H. Lee, and R. P. Wharton (2007)
Development 134, 1519-1527
   Abstract »    Full Text »    PDF »
nanos function is essential for development and regeneration of planarian germ cells.
Y. Wang, R. M. Zayas, T. Guo, and P. A. Newmark (2007)
PNAS 104, 5901-5906
   Abstract »    Full Text »    PDF »
Functional redundancy among Nanos proteins and a distinct role of Nanos2 during male germ cell development.
A. Suzuki, M. Tsuda, and Y. Saga (2007)
Development 134, 77-83
   Abstract »    Full Text »    PDF »
Gene Expression Dynamics During Germline Specification in Mice Identified by Quantitative Single-Cell Gene Expression Profiling.
Y. Yabuta, K. Kurimoto, Y. Ohinata, Y. Seki, and M. Saitou (2006)
Biol Reprod 75, 705-716
   Abstract »    Full Text »    PDF »
E-Cadherin Regulates Human Nanos1, which Interacts with p120ctn and Induces Tumor Cell Migration and Invasion..
K. Strumane, A. Bonnomet, C. Stove, R. Vandenbroucke, B. Nawrocki-Raby, E. Bruyneel, M. Mareel, P. Birembaut, G. Berx, and F. van Roy (2006)
Cancer Res. 66, 10007-10015
   Abstract »    Full Text »    PDF »
Ovarian follicle development and transgenic mouse models.
K.R. Barnett, C. Schilling, C.R. Greenfeld, D. Tomic, and J.A. Flaws (2006)
Hum. Reprod. Update 12, 537-555
   Abstract »    Full Text »    PDF »
Murine homologues of the Drosophila gustavus gene are expressed in ovarian granulosa cells..
Y. Xing, R. Gosden, P. Lasko, and H. Clarke (2006)
Reproduction 131, 905-915
   Abstract »    Full Text »    PDF »
Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish.
T. Okutsu, K. Suzuki, Y. Takeuchi, T. Takeuchi, and G. Yoshizaki (2006)
PNAS 103, 2725-2729
   Abstract »    Full Text »    PDF »
Genomic and Expression Profiling of Human Spermatocytic Seminomas: Primary Spermatocyte as Tumorigenic Precursor and DMRT1 as Candidate Chromosome 9 Gene.
L. H.J. Looijenga, R. Hersmus, A. J.M. Gillis, R. Pfundt, H. J. Stoop, R. J.H.L.M. van Gurp, J. Veltman, H. B. Beverloo, E. van Drunen, A. Geurts van Kessel, et al. (2006)
Cancer Res. 66, 290-302
   Abstract »    Full Text »    PDF »
How different is Venus from Mars? The genetics of germ-line stem cells in Drosophila females and males.
L. Gilboa and R. Lehmann (2004)
Development 131, 4895-4905
   Abstract »    Full Text »    PDF »
Localization of RNAs to the Mitochondrial Cloud in Xenopus Oocytes through Entrapment and Association with Endoplasmic Reticulum.
P. Chang, J. Torres, R. A. Lewis, K. L. Mowry, E. Houliston, and M. L. King (2004)
Mol. Biol. Cell 15, 4669-4681
   Abstract »    Full Text »    PDF »
Nanos suppresses somatic cell fate in Drosophila germ line.
Y. Hayashi, M. Hayashi, and S. Kobayashi (2004)
PNAS 101, 10338-10342
   Abstract »    Full Text »    PDF »
Experimental approaches to the study of primordial germ cell lineage and proliferation.
M. De Felici, M.L. Scaldaferri, M. Lobascio, S. Iona, V. Nazzicone, F.G. Klinger, and D. Farini (2004)
Hum. Reprod. Update 10, 197-206
   Abstract »    Full Text »    PDF »
Spontaneous differentiation of germ cells from human embryonic stem cells in vitro.
A. T. Clark, M. S. Bodnar, M. Fox, R. T. Rodriquez, M. J. Abeyta, M. T. Firpo, and R. A. R. Pera (2004)
Hum. Mol. Genet. 13, 727-739
   Abstract »    Full Text »    PDF »
Nanos Maintains Germline Stem Cell Self-Renewal by Preventing Differentiation.
Z. Wang and H. Lin (2004)
Science 303, 2016-2019
   Abstract »    Full Text »    PDF »
Mechanism of Mouse Germ Cell Specification: A Genetic Program Regulating Epigenetic Reprogramming.
M.A. SURANI, K. ANCELIN, P. HAJKOVA, U.C. LANGE, B. PAYER, P. WESTERN, and M. SAITOU (2004)
Cold Spring Harb Symp Quant Biol 69, 1-10
   Abstract »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)