Abstract
Siah-2 is one of three murine homologues of the Drosophila gene seven in absentia (sina). The sina protein is nuclear localizing and required downstream of Ras1, Raf and the tyrosine kinase sevenless in Drosophila. Recent results have demonstrated a high degree of functional conservation between vertebrate and insect tyrosine kinase signalling pathways, involving such proteins as Son of sevenless, Grb2 and GAP. These findings, together with the high degree of sequence conservation between the Siah proteins and sina, suggest that the mammalian Siah proteins may also participate in signal transduction by some tyrosine kinases. Here, we report a high level of expression of Siah-2 in a specific population of germ cells within both the mouse ovary and testis. Siah-2 expression was absent in primordial oocytes but was detected in all growing oocytes, coincident with their recruitment from the pool of quiescent cells. The level of Siah-2 mRNA increased as the oocytes matured and was readily detectable in Graafian follicles and in fertilized zygotes up until the two cell stage, a time of extensive maternal transcript degradation and zygotic gene activation. The expression of Siah-2 in the testis was first detected in postmeiotic spermatids. These represented a comparable stage of germ cell development to those cells first expressing Siah-2 in the ovary. The expression pattern of Siah-2 in germ cells was similar to that described for the proto-oncogene c-mos, and the possibility that Siah-2 lies downstream of p39mos in signal transduction within the mouse oocyte requires further investigation. Finally, expression of Siah-2 appears to be an excellent marker for the inception of gonadotrophin-independent oocyte growth.
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References
Bachvarova R (1985) Gene expression during oogenesis and oocyte development in mammals. In: Browder LW (ed) Developmental biology: a comprehensive synthesis. Plenum Press, New York, pp 453–524
Baker TG (1982) Oogenesis and ovulation. In: Austin CR, Short RV (eds) Germ cells in fertilization. Cambridge University Press, Cambridge, pp 17–45
Bancroft JD, Stevens A (1982) Theory and practice of histological techniques, 2nd edn. Churchill Livingstone, New York
Bellvé AR (1979) The molecular biology of mammalian spermatogenesis. In: Finn CA (ed) Oxford reviews of reproductive biology. Clarendon Press, Oxford, pp 159–261
Bellvé AR, Caviccia JC, Millette CF, O'Brien AD, Bhatnagar YM, Dym M (1977) Spermatogenic cells of the prepuberal mouse. J Cell Biol 74:68–85
Biggs WH III, Zipursky SL (1992) Primary structure, expression, and signal-dependent tyrosine phosphorylation of a Drosophila homolog of extracellular signal-regulated kinase. Proc Natl Acad Sci USA 89:6295–6299
Borum K (1961) Oogenesis in the mouse: a study of the meiotic prophase. Exp Cell Res 24:495–507
Bowtell D, Fu P, Simon M, Senior P (1992) Identification of murine homologues of the Drosophila Son of sevenless gene; potential activators of ras. Proc Natl Acad Sci USA 89:6511–6515
Braun RE (1990) Temporal translational regulation of the protamine 1 gene during mouse spermatogenesis. Enzyme 44:120–128
Byskov AG (1982) Primordial germ cells and regulation of meiosis. In: Austin CR, Short RV (eds) Germ cells in fertilization. Cambridge University Press, Cambridge, pp 1–16
Carthew RW, Rubin GM (1990) seven in absentia, a gene required for specification of R7 cell fate in the Drosophila eye. Cell 63:561–577
Chiquoine AD (1960) The development of the zona pellucida of the mammalian ovum. Am J Anat 106:149–169
Della NG, Senior PV, Bowtell DDL (1993) Isolation and characterisation of murine homologues of the Drosophila seven in absentia gene (sina). Development 117:1333–1343
Dickson B, Sprenger F, Morrison D, Hafen E (1992) Raf functions downstream of Ras1 in the sevenless signal transduction pathway. Nature 360:600–603
Fabian JR, Morrison DK, Daar IO (1993) Requirement for Raf and MAP kinase function during the meiotic maturation of Xenopus oocytes. J Cell Biol 122(3):645–652
Flach G, Johnson MH, Braude PR, Taylor RAS, Bolton VN (1982) The transition from maternal to embryonic control in the 2-cell mouse embryo. EMBO J 1:681–686
Fortini ME, Simon MA, Rubin GM (1992) Signalling by the sevenless protein kinase is mimicked by Ras1 activation. Nature 355:559–561
Freemont PS (1993) The RING finger: a novel protein sequence motif related to the zinc finger. Ann NY Acad Sci 684:174–192
Gale NW, Kaplan S, Lowenstein EJ, Schlessinger J, Bar-Sagi D (1993) Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363:88–92
Gaul U, Mardon G, Rubin GM (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the sevenless receptor tyrosine kinase. Cell 68:1007–1019
Goldman DS, Kiessling AA, Millette CF, Cooper GM (1987) Expression of c-mos RNA in germ cells of male and female mice. Proc Natl Acad Sci USA 84:4509–4513
Hecht NB (1986) Gene expression during spermatogenesis. In: Rossant J, Pederson RA (eds) Experimental approaches to mammalian embryonic development. Cambridge University Press, Cambridge, pp 151–193
Hogan BLM, Constantini F, Lacy E (1986) Manipulating the mouse embryo: a lab manual. Cold Spring Harbor Laboratory, Cold Spring Harbor
Iwaoki Y, Matsuda H, Mutter GL, Watrin F, Wolgemuth DJ (1993) Differential expression of the proto-oncogenes c-abl and c-mos in developing mouse germ cells. Exp Cell Res 206:212–219
Johnson MH (1981) The molecular and cellular basis of preimplantation mouse development. Biol Rev 56:463–498
Li N, Batzer B, Daly R, Yajnik V, Skolnik E, Chardin P, Bar-Sagi D, Margolis B, Schlessinger J (1993) Guanine-nucleotide-releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363:85–88
Meijer D, Hermans A, Lindern M von, Agthoven T van, Klein A de, Mackenbach P, Grootegoed A, Talarico D, Della Valle G, Grosveld G (1987) Molecular characterization of the testis specific c-abl mRNA in mouse. EMBO J 6:4041–4048
Muslin AJ, MacNicol AM, Williams LT (1993) Raf-1 protein kinase is important for progesterone-induced Xenopus oocyte maturation and acts downstream of mos. Mol Cell Biol 13(7):4197–4202
Mutter GL, Wolgemuth DJ (1987) Distinct developmental patterns of c-mos protooncogene expression in female and male mouse germ cells. Proc Natl Acad Sci USA 84:5301–5305
O'Keefe SJ, Wolfes H, Kiessling AA, Cooper GM (1989) Microinjection of antisense c-mos oligonucleotides prevents meiosis II in the maturing mouse egg. Proc Natl Acad Sci USA 86:7038–7042
Oakberg EF (1956) A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Am J Anat 99:391–413
Olivier JP, Raabe T, Henkemeyer M, Dickson B, Mbamalu G, Margolis B, Schlessinger J, Hafen E, Pawson T (1993) A Drosophila SH2–SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73:179–191
Pawson T, Schlessinger J (1993) SH2 and SH3 domains. Curr Biol 3:434–442
Pedersen T, Peters H (1968) Proposal for a classification of oocytes and follicles in the mouse ovary. J Reprod Fertil 17:555–557
Pelech SL, Sanghera JS (1992) MAP kinases: charting the regulatory pathways. Science 257:1355–1356
Peters H, McNatty KP (1980) The ovary. University of California Press, Berkeley
Ponzetto C, Wolgemuth DJ (1985) Haploid expression of a unique c-abl transcript in the mouse male germ line. Mol Cell Biol 5:1791–1794
Roberts TM (1992) A signal chain of events. Nature 360:534–535
Roosen-Runge EC (1962) The process of spermatogenesis in mammals. Biol Rev 37:343–377
Roosen-Runge EC, Giesel LO (1950) Quantitative studies on spermatogenesis in the albino rat. Am J Anat 87:1–30
Rozakis-Adcock M, Fernley R, Wade J, Pawson T, Bowtell D (1993) The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature 363:83–85
Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF (1988) Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature 335:519–525
Schultz RM (1986) Molecular aspects of mammalian oocyte growth and maturation. In: Rossant R, Pedersen RA (eds) Experimental approaches to mammalian embryonic development. Cambridge University Press, Cambridge, pp 195–237
Schultz RM (1993) Regulation of zygotic gene activation in the mouse. BioEssays 15:531–538
Setchell BP (1978) The mammalian testis. Paul Elek, London
Simon MA, Bowtell DDL, Dodson GS, Laverty TR, Rubin GM (1991) Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701–716
Simon MA, Dodson GS, Rubin GM (1993) An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to seven-less and Sos proteins in vitro. Cell 73:169–177
Wassarman PM, Kinloch RA (1992) Gene expression during oogenesis in mice. Mut Res 296:3–15
Williams LT (1992) Missing links between receptors and Ras. Curr Biol 2:601–603
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Della, N.G., Bowtell, D.D.L. & Beck, F. Expression of Siah-2, a vertebrate homologue of Drosophila sina, in germ cells of the mouse ovary and testis. Cell Tissue Res 279, 411–419 (1995). https://doi.org/10.1007/BF00318499
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DOI: https://doi.org/10.1007/BF00318499