XY chromosomal bivalent: Nucleolar attraction

Abstract

Nucleolar organization by autosomal bivalents occurs during male meiotic prophase in mammalian species. During late leptotene-early zygotene stages, several autosomal bivalents are engaged in ribosomal RNA synthesis. At pachytene stage, nucleolar masses detach from the sites of primary autosomal origin, relocate close to the XY chromosomal pair, and nucleolar components become segregated. In early pachytene, an extensive synaptonemal complex at the pseudoautosomal region, links X and Y chromosomes in close juxtaposition along most of the length of the Y chromosome, except for a terminal region of the Y that diverges from the pairing region. As meiotic prophase advances, X and Y chromosomes progressively desynapse and, at diplotene, the XY pair is associated end-to-end. Xmr (Xlr-related, meiosis regulated) is a protein component of the nucleolus associated to the XY pair and of the asynapsed portions of the X and Y axial cores. Xmr, like SCP3, is a component of the lateral element of the synaptonemal complex. Both share structural homology in their C-terminal region. This region contains several putative coiled-coil domains known to mediate heterodimeric protein-protein interactions and to provide binding sites to regulatory proteins. Like Xmr, the tumor repressor protein BRCA1 is present along the unsynapsed cores of the XY bivalent. Both Xmr and BRCA1 have been implicated in a mechanism leading to chromatin condensation and transcription inactivation of the XY bivalent. The BRCA1-ATR kinase complex, as recent research suggests, triggers the phosphorylation of histone H2AX, which predominates in the condensed chromatin of the XY chromosomal pair. Xmr is not present in the XY bivalent when the expression of histone H2AX is deficient. The role of Xmr in chromatin condensation of the XY bivalent has not been determined. The partial structural homology of SCP3 and Xmr, their distribution along the unsynapsed axial cores of the X and Y chromosomes, and the presence of Xmr in the XY pair-associated nucleolus raises the possibility that Xmr, and other proteins including protein kinases, may be recruited to the nucleolus to perform functions related to chromosomal synapsis, chromatin condensation and recombination processes, as well as cell cycle progression. Mol. Reprod. Dev. 72: 1-6, 2005. ß 2005 Wiley-Liss, Inc.

Mammalian neo-oogenesis and expression of meiosis-specific protein SCP3 in adult human and monkey ovaries

“…J-L in Figure 1 show SCP3 expression in developing rat testes (positive control). Note SCP3 immunostaining of spermatogonial nucleoli in the 3-day-old rat (arrowhead, J), which is characteristic for early stages of meiotic prophase 13 and resembles observations in primordial follicle oocytes of postovulatory adult human and monkey ovaries (see Fig. 1F-H).…”

“…Recently, Tres reported that male germ cells exhibit nucleolar SCP3 expression during early stages of meiotic prophase. 13 In addition, an SCP3+ synapsis of two chromosomes was detected in human primordial follicle oocytes (arrowhead, H and insert), possibly representing XX chromosomal synapsis, since sex chromosomes start synapsis during early zygotene, before autosomes synapse. 13 Observations from twelve human cases studied are summarized in Table 1.…”

“…13 In addition, an SCP3+ synapsis of two chromosomes was detected in human primordial follicle oocytes (arrowhead, H and insert), possibly representing XX chromosomal synapsis, since sex chromosomes start synapsis during early zygotene, before autosomes synapse. 13 Observations from twelve human cases studied are summarized in Table 1. Rare SCP3+ oocytes (less then 10%) were detected in midfollicular phase ovaries (case #1).…”

Ovarian Stem Cell Niche and Follicular Renewal in Mammals

“…Moreover, the SCP3 immunostaining was observed in the nucleoli of oocytes in some primordial follicles in human (arrowhead, panel F) and monkey ovaries (white arrowhead, panel G). Tres reported that male germ cells exhibit nucleolar SCP3 expression during early stages of meiotic prophase (Tres, 2005). In addition, an SCP3 þ synapsis of two chromosomes was detected in human primordial follicle oocyte (arrowhead, panel H and insert), possibly representing XX chromosomal synapsis, since sex chromosomes start synapsis during early zygotene, before autosomes synapse (Tres, 2005).…”

“…Tres reported that male germ cells exhibit nucleolar SCP3 expression during early stages of meiotic prophase (Tres, 2005). In addition, an SCP3 þ synapsis of two chromosomes was detected in human primordial follicle oocyte (arrowhead, panel H and insert), possibly representing XX chromosomal synapsis, since sex chromosomes start synapsis during early zygotene, before autosomes synapse (Tres, 2005). Rare SCP3 þ oocytes (<10%) were detected in midfollicular phase ovaries.…”