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Left-Right Asymmetry in Chicken Embryonic Gonads

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Left-Right Asymmetry in Chicken Embryonic Gonads http://www.jstage.jst.go.jp/browse/jpsa doi:10.2141/ jpsa.0140032 Copyright Ⓒ 2014, Japan Poultry Science Association. ≪Review≫ Left-Right Asymmetry in Chicken Embryonic Gonads Sittipon Intarapat1 andClaudioD.Stern2 1 Department of Anatomy, Faculty of Science, Mahidol University, Bangkok 10400, Thailand 2 Department of Cell and Developmental Biology and UCL Centre for Stem Cells and Regenerative Medicine, University College London, Gower Street, London WC1E 6BT, UK. Avian embryos have reproductive organs with unique characteristics. In female, the gonads develop asymmetrically: the left gonad generates a functional ovary, whereas the right gonad and associated embryonic oviduct (Müllerian duct) regress. In males, however, both left and right gonads develop into testes. Recent evidence, however, revealed that left-right asymmetry can be detected in both sexes. Even male embryos have a greater number of germ cells in the left gonad. Moreover, pluripotency-associated markers, as well as SSEA1, the surface antigen that is strongly expressed in chick embryonic stem cells, also show asymmetric expression in both sexes both in germ cells and in stromal cells of the gonad. This review provides an update of the state of the field. Key words: chick, gonads, left-right asymmetry, PGCs, pluripotent stem cell markers J. Poult. Sci., 51: 352-358, 2014 Introduction Gonadogenesis and Left-right Asymmetry of Embryonic Gonads During embryonic development, left-right asymmetry of some organs is associated with several processes such as During development of the gonads, the intermediate embryonic turning, forming and patterning of visceral organs mesoderm starts to form a rod-shaped structure situated (Levin, 2005; Raya and Izpisua Belmonte, 2006). A number between the paraxial and lateral plate mesoderm. A pair of of genes encoding transcription factors and secreted growth rod-shaped-structure then rapidly proliferate giving rise to factors play a crucial role in these processes; some differ paired bulged structures called “the genital or gonadal among different species whereas a few are strongly ridges”. These ridges locate medioventrally on the meso- conserved. Two of the key factors, Pitx2 and Nodal, are nephros (Romanoff, 1960; McCarrey and Abbott, 1979; conserved in all vertebrates and perhaps even in all events Rodemer et al., 1986). It has been reported that thickening that establish left-right asymmetry in embryogenesis (Levin of the mesenchymal blastema of the genital ridges, with et al., 1995; Ryan et al., 1998; Yoshioka et al., 1998; Zhu et contributions from the coelomic epithelium and mesonephros al., 1999; Levin, 2005). PITX2 is a homeobox-containing resulted in a group of differentiated cells in the gonads transcription factor with a bicoid-type homeodomain, (Bishop-Calame, 1966; Carlon et al., 1983; Merchant- whereas Nodal is a secreted protein of the TGFβ superfamily. Larios et al., 1984; Carlon and Stahl, 1985; Ukeshima et al., Their expression patterns have been found in the left lateral 1987; Martineau et al., 1997). At the beginning of plate mesoderm during the development of heart and head gonadogenesis, the gonads of both sexes are not yet to be (Gage et al., 1999a, b; Zhu et al., 1999) and generally on the distinguished by gonadal morphology so called the “indiffer- left side of every organ system that show left-right asym- ent stage” (McCarrey and Abbott, 1979; Clinton, 1998; metry in vertebrates. Pitx2-knockout mice have abnormal- Clinton and Haines, 2001). Thereafter, the indifferent ities of internal organ asymmetry (Lin et al., 1999; Lu et al., gonads enter to sexual differentiation in which male and 1999). Recently, Pitx2 was reported to play a role in em- female gonadal ridges differentiate into the testes and bryonic gonad asymmetry in both sexes (Guioli and Lovell- ovaries, respectively (Clinton, 1998; Clinton and Haines, Badge, 2007; Ishimaru et al., 2008; Rodriguez-Leon et al., 2001; Smith and Sinclair, 2004; Smith et al., 2007; Smith, 2008). 2010; Chue and Smith, 2011; Ayers et al., 2013). The somatic cells in the gonadal ridges become steroidogenic or Received: February 22, 2014, Accepted: April 15, 2014 Released Online Advance Publication: May 25, 2014 hormone producing cells and supporting cells in both sexes Correspondence: Dr. S. Intarapat, Department of Anatomy, Faculty of (Merchant-Larios et al., 1984; Merchant-Larios et al., 1993). Science, Mahidol University, Bangkok 10400, Thailand. Primordial germ cells (PGCs) are surrounded by these (E-mail: [email protected]) somatic cells and therefore further develop into primary sex Intarapat and Stern: Gonadal Asymmetry in Chicken Embryos 353 cords (Romanoff, 1960; Stahl and Carlon, 1973; McCarrey ovary (Romanoff, 1960; Smith and Sinclair, 2001; Smith and Abbott, 1979). Like mammalian gonads, chicken and Sinclair, 2004). There is no further development of the embryonic gonads consist of two layers, the outer cortex and right gonad and this leads to the formation of vestigial inner medulla (Maraud et al., 1987; Clinton, 1998; Clinton structures (Carlon and Stahl, 1985) or complete regression and Haines, 2001; Smith and Sinclair, 2004). Development (Romanoff, 1960) at the adult stage. The molecular of the primary sex cords differs in the two sexes: embryonic mechanism underlying asymmetrical development and the ovaries develop from the cortex, while the testes develop degeneration of the right ovary in female birds relies on from the medulla (Romanoff, 1960; McCarrey and Abbott, PITX2 (Guioli and Lovell-Badge, 2007; Ishimaru et al., 1979; Maraud et al., 1987). In developing testes, cell divi- 2008; Rodriguez-Leon et al., 2008). Guioli and Lovell- sion in the medulla is faster than that in the cortex leading Badge (2007) demonstrated that misexpression of Pitx2 in to the thinning of the cortex in male gonads and vice versa the right gonad using transfection with the RCAS retroviral (Romanoff, 1960; McCarrey and Abbott, 1979; Clinton, vector is sufficient not only to induce symmetric develop- 1998). Furthermore, the medullary cords further develop ment of the gonads but also to rescue the degeneration of the into secondary sex cords (testicular cords in male) right ovary. A later experiment using a similar method (Romanoff, 1960; Stahl and Carlon, 1973; McCarrey and demonstrated that RCAS-Pitx2 transfected gonads exhibits Abbott, 1979). Conversely, in developing ovaries, the cor- symmetric distribution of a number of Vasa and Oct4 tical cords further develop; whereas the medullary cords positive cells in both left and right genital ridges compared to regress resulted in secondary sex cord development giving wild-type embryos at stage 20 HH (Rodriguez-Leon et al., rise to the thick cortex in female left ovary (Romanoff, 1960; 2008), along with retention of the right ovary in female Stahl and Carlon, 1973; McCarrey and Abbott, 1979). embryos at stage 34 HH (Rodriguez-Leon et al., 2008). Gonadal differentiation is controlled by the genes located on These findings reveal a pivotal role of PITX2 in germ cell sex chromosomes (Stevens, 1997; Smith and Sinclair, 2001; survival in the right gonad as well as restoration of the right Smith and Sinclair, 2004; Smith et al., 2007; Smith, 2010; gonad from degeneration in female embryos. Chue and Smith, 2011; Ayers et al., 2013). In addition, two Asymmetric Germ Cell Distribution in independent mechanisms including the genetic cascade Female and Male Embryonic Gonads regulating cellular differentiation and the sex-determining mechanism controlling the differentiation of the gonadal Asymmetric germ cell distribution in chicken embryos ridges have been proposed (Clinton, 1998; Clinton and was first reported in 1935 by Witschi (Witschi, 1935); since Haines, 2001; Smith and Sinclair, 2001; Smith and Sinclair, then, it has been described that the number of PGCs in the 2004; Smith et al., 2007; Smith, 2010; Chue and Smith, left gonad is greater than that in the right gonad. Other 2011; Ayers et al., 2013). In summary, gonadogenesis in previous studies also supported that the left gonadal ridges male and female embryos is so called medullary and cortical contain more germ cells than the right side in female em- development, respectively (Romanoff, 1960; McCarrey and bryos (Van Limborgh, 1954; Van Limborgh, 1968; Van Abbott, 1979). Limborgh, 1970; Vallisneri et al., 1990; Zaccanti et al., 1990). Unlike mammals, which have apparently symmetric It is not yet clear what actually controls asymmetric germ cell gonads, most female bird species develop asymmetrically, distribution. It is possible that chemotactic and/or mitogenic generating a functional ovary only on the left side, whereas factors play a role in germ cells migration, and it has been males develop bilateral testes (Romanoff, 1960). Gonadal proposed that the left gonadal ridge secretes such factors asymmetry has been reported in several avian species more than the right, leading to increased PGCs migration including duck (Van Limborgh and Van Faassen, 1960; Van and/or division in the left gonad (Witschi, 1935; Swartz and Limborgh, 1970), turkey (Burke, 1973) and chicken (Van Domm, 1972). One study supported this by showing that Limborgh, 1954; Van Limborgh, 1960; Hocking, 1992; engrafted quail PGCs differentially colonized the left and Calhim and Birkhead, 2009). This asymmetry can be related right presumptive gonads at limb bud stages (HH 18-24) to the results of gonad growth (Mittwoch et al., 1971; (Didier and Fargeix, 1976). This phenomenon was also seen Mittwoch
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