The Synaptonemal Complex Protein SCP3 Can Form Multistranded, Cross-striated Fibers In Vivo

Abstract

The synaptonemal complex protein SCP3 is part of the lateral element of the synaptonemal complex, a meiosis-specific protein structure essential for synapsis of homologous chromosomes. We have investigated the fiber-forming properties of SCP3 to elucidate its role in the synaptonemal complex. By synthesis of SCP3 in cultured somatic cells, it has been shown that SCP3 can self-assemble into thick fibers and that this process requires the COOH-terminal coiled coil domain of SCP3, as well as the NH2-terminal nonhelical domain. We have further analyzed the thick SCP3 fibers by transmission electron microscopy and immunoelectron microscopy. We found that the fibers display a transversal striation with a periodicity of ∼20 nm and consist of a large number of closely associated, thin fibers, 5–10 nm in diameter. These features suggest that the SCP3 fibers are structurally related to intermediate filaments. It is known that in some species the lateral elements of the synaptonemal complex show a highly ordered striated structure resembling that of the SCP3 fibers. We propose that SCP3 fibers constitute the core of the lateral elements of the synaptonemal complex and function as a molecular framework to which other proteins attach, regulating DNA binding to the chromatid axis, sister chromatid cohesion, synapsis, and recombination.

Evolutionary history of the mammalian synaptonemal complex

“…Especially the central domain and two previously identified flanking motifs -CM1 and CM2 10 -exhibit a high degree of sequence conservation in a comparison of vertebrate protein sequences (Baier et al 2007b). Ectopic expression of SYCP3 revealed that the protein is able to assemble to higher order filaments and networks in the heterologous system of somatic COS-7 cells which resemble the basic fibrils of the AEs/LEs (Yuan et al 1998;Baier et al 2007b). The conserved region was thereby found to be necessary and sufficient for this polymerization process (Baier et al 2007b).…”

“…as bona fide structural components of the LEs and TFs, therefore, seems to be undisputable and their emergence in the ancestor of metazoans is logically consistent. At least in vitro, the mammalian SYCP1 and SYCP3 do not require additional components to polymerize to higher order structures which already resemble the respective SC domains pointing to their significance in the assembly process (Yuan et al 1998;Öllinger et al 2005). In vivo, the proper localization of the mammalian SYCP3 is influenced by the presence of SYCP2 (Yang et al 2006).…”

The T657C polymorphism on the SYCP3 gene is associated with recurrent pregnancy loss

“…Therefore, it was suggested that SYCP1 gene had a coordinating role in synapse formation as well as homologous chromosomes pairing [14]. In 2002, Li Yuan et al conducted a comprehensive study on mouse SYCP3 gene: high expression of SYCP3 protein in SC demonstrates its strong role in this complex [15].…”

SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division

“…Several experimental results suggest that these proteins are structural elements of the AE (for review, see Page and Hawley, 2004). Ectopic production of SYCP3 in mammalian somatic-cell-culture cells gives rise to extended AE-like fibres (Yuan et al, 1998). Furthermore, ultrastructural light-microscopy studies of Sycp3-deficient male and female germ cells have revealed a complete loss of the nuclear silverstained filaments normally associated with the SC (Yuan et al, 2002;Yuan et al, 2000).…”