Abstract
BackgroundTelomeres 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.ResultsWe 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.ConclusionCCDC79 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.
Highlights
Telomeres have crucial meiosis-specific roles in the orderly reduction of chromosome numbers and in ensuring the integrity of the genome during meiosis
RAP1 is a constitutive component of mammalian telomeres and is the predicted mammalian orthologue of spRap1, it is not required for telomere-nuclear envelope (NE) interaction in mice [12], SUN-domain proteins, SUN1 [13] and possibly SUN2 [14,15], are required for tethering telomeres to the NE during meiosis in mice
Expression of Ccdc79 is restricted to male and female meiotic germ cells To identify uncharacterised proteins that are possibly involved in meiotic chromosome biology, we screened for mouse genes whose expression is upregulated in the developing gonads upon entry of germ cells into the first meiotic prophase in both sexes
Summary
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. RAP1 is a constitutive component of mammalian telomeres and is the predicted mammalian orthologue of spRap, it is not required for telomere-NE interaction in mice [12], SUN-domain proteins, SUN1 [13] and possibly SUN2 [14,15], are required for tethering telomeres to the NE during meiosis in mice These two proteins are present in the inner NE both in somatic and meiotic cells. Meiosis-specific modifications to constitutive telomere proteins, or additional meiosis-specific telomere components, must exist in order to establish telomere-NE attachments in mammalian meiocytes
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