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Open Access Research article

Mouse CCDC79 (TERB1) is a meiosis-specific telomere associated protein

Katrin Daniel1, Daniel Tränkner1, Lukasz Wojtasz1, Hiroki Shibuya2, Yoshinori Watanabe2, Manfred Alsheimer3 and Attila Tóth1*

Author Affiliations

1 Institute of Physiological Chemistry, Technische Universität Dresden, Fiedlerstr. 42, Dresden 01307, Germany

2 Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, Japan

3 Department of Cell and Developmental Biology, Biocenter, University of Würzburg, AmHubland, Würzburg 97074, Germany

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BMC Cell Biology 2014, 15:17  doi:10.1186/1471-2121-15-17

Published: 22 May 2014

Abstract

Background

Telomeres have crucial meiosis-specific roles in the orderly reduction of chromosome numbers and in ensuring the integrity of the genome during meiosis. One such role is the attachment of telomeres to trans-nuclear envelope protein complexes that connect telomeres to motor proteins in the cytoplasm. These trans-nuclear envelope connections between telomeres and cytoplasmic motor proteins permit the active movement of telomeres and chromosomes during the first meiotic prophase. Movements of chromosomes/telomeres facilitate the meiotic recombination process, and allow high fidelity pairing of homologous chromosomes. Pairing of homologous chromosomes is a prerequisite for their correct segregation during the first meiotic division. Although inner-nuclear envelope proteins, such as SUN1 and potentially SUN2, are known to bind and recruit meiotic telomeres, these proteins are not meiosis-specific, therefore cannot solely account for telomere-nuclear envelope attachment and/or for other meiosis-specific characteristics of telomeres in mammals.

Results

We identify CCDC79, alternatively named TERB1, as a meiosis-specific protein that localizes to telomeres from leptotene to diplotene stages of the first meiotic prophase. CCDC79 and SUN1 associate with telomeres almost concurrently at the onset of prophase, indicating a possible role for CCDC79 in telomere-nuclear envelope interactions and/or telomere movements. Consistent with this scenario, CCDC79 is missing from most telomeres that fail to connect to SUN1 protein in spermatocytes lacking the meiosis-specific cohesin SMC1B. SMC1B-deficient spermatocytes display both reduced efficiency in telomere-nuclear envelope attachment and reduced stability of telomeres specifically during meiotic prophase. Importantly, CCDC79 associates with telomeres in SUN1-deficient spermatocytes, which strongly indicates that localization of CCDC79 to telomeres does not require telomere-nuclear envelope attachment.

Conclusion

CCDC79 is a meiosis-specific telomere associated protein. Based on our findings we propose that CCDC79 plays a role in meiosis-specific telomere functions. In particular, we favour the possibility that CCDC79 is involved in telomere-nuclear envelope attachment and/or the stabilization of meiotic telomeres. These conclusions are consistent with the findings of an independently initiated study that analysed CCDC79/TERB1 functions.

Keywords:
Meiosis; Telomeres; Telomere attachment; CCDC79; TERB1; SUN1; Nuclear envelope; Recombination; Homologue pairing; Meiotic cohesion; SMC1B