Nuclear Envelope Retention of LINC Complexes Is Promoted by SUN-1 Oligomerization in the Caenorhabditis elegans Germ Line.
SUN (Sad1 and UNC-84) and KASH (Klarsicht, ANC-1, and Syne homology) proteins are constituents of the inner and outer nuclear membranes. They interact in the perinuclear space via C-terminal SUN-KASH domains to form the linker of nucleoskeleton and cytoskeleton (LINC) complex thereby bridging the nuclear envelope. LINC complexes mediate numerous biological processes by connecting chromatin with the cytoplasmic force-generating machinery. Here we show that the coiled-coil domains of SUN-1 are required for oligomerization and retention of the protein in the nuclear envelope, especially at later stages of female gametogenesis. Consistently, deletion of the coiled-coil domain makes SUN-1 sensitive to unilateral force exposure across the nuclear membrane. Premature loss of SUN-1 from the nuclear envelope leads to embryonic death due to loss of centrosome-nuclear envelope attachment. However, in contrast to previous notions we can show that the coiled-coil domain is dispensable for functional LINC complex formation, exemplified by successful chromosome sorting and synapsis in meiotic prophase I in its absence.
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Anahita
A
Daryabeigi
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Alexander
A
Woglar
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Antoine
A
Baudrimont
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Nicola
N
Silva
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Dimitra
D
Paouneskou
Center for Anatomy and Cell Biology, Department of Cell and Developmental Biology, Medical University of Vienna, 1090, Austria.
Cornelia
C
Vesely
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Manuel
M
Rauter
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria.
Alexandra
A
Penkner
Center for Anatomy and Cell Biology, Department of Cell and Developmental Biology, Medical University of Vienna, 1090, Austria.
Michael
M
Jantsch
Department of Chromosome Biology, Max F. Perutz Laboratories, Vienna Biocenter, University of Vienna, 1030, Austria verena.jantsch@univie.ac.at.
Verena
V
Jantsch
D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D005260:Female; D008540:Meiosis; D009685:Nuclear Envelope / Q000378:metabolism*; D009687:Nuclear Proteins / Q000235:genetics / Q000378:metabolism; D009867:Oogonia / Q000378:metabolism*; D011485:Protein Binding; D000072417:Protein Domains; D055503:Protein Multimerization; D018160:Receptors, Cytoplasmic and Nuclear / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
D029742:Caenorhabditis elegans Proteins; D018797:Cell Cycle Proteins; C544270:KDP-1 protein, C elegans; D009687:Nuclear Proteins; D018160:Receptors, Cytoplasmic and Nuclear; C514114:sun-1 protein, C elegans
Caenorhabditis elegans; LINC complex; meiosis; oocyte formation