Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function

Jana Link; Monika Leubner; Johannes Schmitt; Eva Göb; Ricardo Benavente; Kuan-Teh Jeang; Rener Xu; Manfred Alsheimer

doi:10.1371/journal.pgen.1004099

Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function

PLoS Genet. 2014 Feb 27;10(2):e1004099. doi: 10.1371/journal.pgen.1004099. eCollection 2014 Feb.

Authors

Jana Link¹, Monika Leubner¹, Johannes Schmitt¹, Eva Göb¹, Ricardo Benavente¹, Kuan-Teh Jeang², Rener Xu³, Manfred Alsheimer¹

Affiliations

¹ Department of Cell and Developmental Biology, Biocenter, University of Würzburg, Würzburg, Germany.
² Molecular Virology Section, Laboratory of Molecular Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America.
³ Institute of Developmental Biology and Molecular Medicine and School of Life Science, Fudan University, Shanghai, China.

Abstract

LINC complexes are evolutionarily conserved nuclear envelope bridges, composed of SUN (Sad-1/UNC-84) and KASH (Klarsicht/ANC-1/Syne/homology) domain proteins. They are crucial for nuclear positioning and nuclear shape determination, and also mediate nuclear envelope (NE) attachment of meiotic telomeres, essential for driving homolog synapsis and recombination. In mice, SUN1 and SUN2 are the only SUN domain proteins expressed during meiosis, sharing their localization with meiosis-specific KASH5. Recent studies have shown that loss of SUN1 severely interferes with meiotic processes. Absence of SUN1 provokes defective telomere attachment and causes infertility. Here, we report that meiotic telomere attachment is not entirely lost in mice deficient for SUN1, but numerous telomeres are still attached to the NE through SUN2/KASH5-LINC complexes. In Sun1(-/-) meiocytes attached telomeres retained the capacity to form bouquet-like clusters. Furthermore, we could detect significant numbers of late meiotic recombination events in Sun1(-/-) mice. Together, this indicates that even in the absence of SUN1 telomere attachment and their movement within the nuclear envelope per se can be functional.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Cell Cycle Proteins / genetics
Cytoskeletal Proteins
Meiosis / genetics*
Membrane Proteins / genetics*
Mice
Microtubule-Associated Proteins / genetics*
Multiprotein Complexes / genetics
Nuclear Envelope / genetics
Nuclear Proteins / genetics
RNA, Long Noncoding / genetics*
Telomere / genetics
Telomere-Binding Proteins / genetics*

Substances

Cell Cycle Proteins
Cytoskeletal Proteins
KASH5 protein, mouse
Membrane Proteins
Microtubule-Associated Proteins
Multiprotein Complexes
Nuclear Proteins
RNA, Long Noncoding
SUN1 protein, mouse
Sun2 protein, mouse
Telomere-Binding Proteins

Grants and funding

This study was supported by the German Research Foundation (DFG, http://www.dfg.de), grant Al 1090/2-1 (Priority Program SPP1384 “Mechanisms of genome haploidization”) to MA, and the Graduate School GK1048 of the University of Würzburg (http://www.gk-1048.uni-wuerzburg.de). It received further funding by the German Research Foundation (DFG) and the University of Würzburg in the funding programme Open Access Publishing. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.