Abstract
The protein of the gustavus (gus) gene has a typical SOCS box domain and repeats in the splA and RyR (SPRY) domains. GUS can interact with Vasa and is necessary for the specification of germ cells. We cloned two zebrafish genes, SSB-1 and SSB-4 (SPRY domain SOCS box proteins). Phylogenetic analysis shows that zebrafish SSB-1 and SSB-4 are clustered into clades of SSB-1-like and SSB-4-like genes from other species. RT-PCR analysis of tissues revealed that zebrafish SSB-1 and -4 are expressed in the ovary and testis. We investigated the spatial expression patterns of zebrafish SSB-1 and -4 in embryos from the two-cell stage to 72 h postfertilization (hpf) using whole-mount in situ hybridization. SSB-1 and -4 transcripts were present in all blastomeres during the early embryonic stages, but the genes differ in their expression pattern. SSB-4 mRNA was located in the region of the primordial germ cells in 24 and 72 hpf embryos, but SSB-1 mRNA was not detected at these stages. We hypothesize that SSB-4 plays a role in the early development of germ cells.
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References
Eddy EM (1975) Germ plasm and the differentiation of the germ cell line. Int Rev Cytol 43:229–280
Fausto AM, Picchietti S, Taddei AR, Zeni C, Scapigliati G, Mazzini M, Abelli L (2004) Formation of the egg envelope of a teleost, Dicentrarchus labrax (L.): immunochemical and cytochemical detection of multiple components. Anat Embryol (Berl) 208(1):43–53
Hilton DJ, Richardson RT, Alexander WS, Viney EM, Willson TA, Sprigg NS, Starr R, Nicholson SE, Metcalf D, Nicola NA (1998) Twenty proteins containing a C-terminal SOCS box form five structural classes. Proc Natl Acad Sci USA 95(1):114–119
Kamura T, Sato S, Haque D, Liu L, Kaelin WG Jr, Conaway RC, Conaway JW (1998) The Elongin BC complex interacts with the conserved SOCS-box motif present in members of the SOCS, ras, WD-40 repeat, and ankyrin repeat families. Genes Dev 12:3872–3881
Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
Koprunner M, Thisse C, Thisse B, Raz E (2001) A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev 15:2877–2885
Mahowald AP (1992) Germ plasm revisited and illuminated. Science 255:1216–1217
Masters SL, Palmer KR, Stevenson WS, Metcalf D, Viney EM, Sprigg NS, Alexander WS, Nicola NA, Nicholson SE (2005) Genetic deletion of murine SPRY domain-containing SOCS box protein 2 (SSB-2) results in very mild thrombocytopenia. Mol Cell Biol 25:5639–5647
Olsen LC, Aasland R, Fjose A (1997) A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 66:95–105
Parrott JA, Skinner MK (1998) Developmental and hormonal regulation of keratinocyte growth factor expression and action in the ovarian follicle. Endocrinology 139:228–235
Pelegri F, Knaut H, Maischein HM, Schulte-Merker S, Nusslein-Volhard C (1999) A mutation in the zebrafish maternal-effect gene nebel affects furrow formation and vasa RNA localization. Curr Biol 9:1431–1440
Ramasamy S, Wang H, Quach HN, Sampath K (2006) Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. Dev Biol 292:393–406
Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55:1141–1163
Schisa JA, Pitt JN, Priess JR (2001) Analysis of RNA associated with P granules in germ cells of C. elegans adults. Development 128:1287–1298
Seydoux G, Strome S (1999) Launching the germline in Caenorhabditis elegans: Regulation of gene expression in early germ cells. Development 126:3275–3283
Strome S (1992) Developmental biology. The germ of the issue. Nature 358:368–369
Styhler S, Nakamura A, Lasko P (2002) VASA localization requires the SPRY-domain and SOCS-box containing protein, GUSTAVUS. Dev Cell 3:865–876
Wang D, Li Z, Messing EM, Wu G (2005) The SPRY domain-containing SOCS box protein 1 (SSB-1) interacts with MET and enhances the hepatocyte growth factor-induced Erk-Elk-1-serum response element pathway. J Biol Chem 280:16393–16401
Weidinger G, Stebler J, Slanchev K, Dumstrei K, Wise C, Lovell-Badge R, Thisse C, Thisse B, Raz E (2003) dead end, a novel vertebrate germ plasm component, is required for zebrafish primordial germ cell migration and survival. Curr Biol 13:1429–1434
Westerfield M (1994) The zebrafish book. University of Oregon Press, Eugene, Oregon
Xing Y, Gosden R, Lasko P, Clarke H (2006) Murine homologs of the Drosophila gustavus gene are expressed in ovarian granulosa cells. Reproduction 131:905–915
Yang XM, Park M (1995) Expression of the hepatocyte growth factor/scatter factor receptor tyrosine kinase is localized to epithelia in the adult mouse. Lab Invest 73:483–491
Yoon C, Kawakami K, Hopkins N (1997) Zebrafish vasa homologue RNA is localized to the cleavage planes of 2- and 4-cell-stage embryos and is expressed in the primordial germ cells. Development 124:3157–3165
Zhang JG, Farley A, Nicholson SE, Willson TA, Zugaro LM, Simpson RJ, Moritz RL, Cary D, Richardson R, Hausmann G, Kile BJ, Kent SB, Alexander WS, Metcalf D, Hilton DJ, Nicola NA, Baca M (1999) The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc Natl Acad Sci USA 96:2071–2076
Acknowledgments
We thank Wenyan Li for thoughtful reading of the manuscript. We also thank members of the Deng lab for helpful discussions and technical assistance. This work was supported by the National Natural Science Foundation of China (grant nos. 30570968 and 30871407), from the ‘‘863 Program’’ (grant no. 2007AA06Z407), and the National personnel training base of basic science education (grant no. J0630648).
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Li, JZ., Zhou, YP., Zhen, Y. et al. Cloning and Characterization of the SSB-1 and SSB-4 Genes Expressed in Zebrafish Gonads. Biochem Genet 47, 179–190 (2009). https://doi.org/10.1007/s10528-008-9215-1
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DOI: https://doi.org/10.1007/s10528-008-9215-1