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. 2007 May 1;104(18):7426-31.
doi: 10.1073/pnas.0609198104. Epub 2007 Apr 23.

Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope

Johannes Schmitt  1 , Ricardo Benavente, Didier Hodzic, Christer Höög, Colin L Stewart, Manfred Alsheimer
Affiliations

Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope

Johannes Schmitt et al. Proc Natl Acad Sci U S A. .

Abstract

Dynamic repositioning of telomeres is a unique feature of meiotic prophase I that is highly conserved among eukaryotes. At least in fission yeast it was shown to be required for proper alignment and recombination of homologous chromosomes. On entry into meiosis telomeres attach to the nuclear envelope and transiently cluster at a limited area to form a chromosomal bouquet. Telomere clustering is thought to promote chromosome recognition and stable pairing of the homologs. However, the molecular basis of telomere attachment and movement is largely unknown. Here we report that mammalian SUN-domain protein Sun2 specifically localizes to the nuclear envelope attachment sites of meiotic telomeres. Sun2-telomere association is maintained throughout the dynamic movement of telomeres. This association does not require the assembly of chromosomal axial elements or the presence of A-type lamins. Detailed EM analysis revealed that Sun2 is part of a membrane-spanning fibrillar complex that interconnects attached telomeres with cytoplasmic structures. Together with recent findings in fission yeast, our study indicates that the molecular mechanisms required for tethering meiotic telomeres and their dynamic movements during bouquet formation are conserved among eukaryotes.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Sun2 localizes to the NE attachment sites of meiotic telomeres. (A) Sun2 (green) shows a homogeneous rim-like pattern within the NE of rat somatic testicular cells. (B–G) Localization of Sun2 in prophase I spermatocytes. Sun2 displays a punctate pattern in pachytene (B–D) as well as leptotene (E), zygotene (F), and diplotene (G) stages. (A′–G′) The same cells were costained for LAP2 or SYCP3 (red). Overlays are seen in A″–G″. All sections were labeled with the DNA-specific fluorochrome Hoechst 33258 (A‴–G‴). Some of the Sun2 spots are denoted by arrows; arrowheads indicate the midplane of nuclei. Images were taken from testis cryosections by confocal laser scanning microscopy, with the exception of D, which represents a whole-cell preparation recorded with wide-field epifluorescence microscopy. (Scale bars: 10 μm.)
Fig. 2.
Fig. 2.
Sun2 localization is independent of A-type lamins and does not require AE/LE assembly. Shown is immunolocalization of Sun2 (green) in spermatocytes (A, B, and D) or somatic testicular cells (C) from wild-type (A), Lmna−/− (B and C), and Sycp3−/− (D) mice. Sections were costained with antibodies against SYCP3 (A–C) or alternatively with CREST serum, which labels centromeres that, in the mouse, are located at one end of each chromosome (D) (red). All sections were labeled with the DNA-specific fluorochrome Hoechst 33258 (A‴–F‴). Overlays are seen in A″–D″. (Scale bars: 10 μm.)
Fig. 3.
Fig. 3.
Immunogold EM examination of Sun2 in mouse spermatocytes. (A) Electron microscopic analysis of a telomere attachment site in pachytene. Ch, chromatin; CE, central element of the SC. (B–D) Electron microscopic immunolocalization of Sun2. Attachment plates are denoted by arrowheads; arrows indicate some of the cytoplasmic fibrils that are attached to the NE. (Scale bar: 100 nm.)
Fig. 4.
Fig. 4.
Model for the organization of the NE at the attachment sites of meiotic chromosomes. In meiotic cells Sun2 is exclusively located at the attachment plates, where it is involved in tethering meiotic telomeres to the NE. Within the perinuclear space its C-terminal SUN domain binds to the KASH domain of nesp2G, thus forming a stable fibrillar complex bridging both nuclear membranes. Because nesp2G interacts with cytoplasmic actin via its actin binding domain, the formation of such a complex would link telomeres to the actin cytoskeleton. This model is consistent with recent findings that identified an actin-dependent mechanism for bouquet formation. AP, attachment plate; CE, central element of the SC; NPC, nuclear pore complex; PNS, perinuclear space; ONM, outer nuclear membrane.
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