期刊论文详细信息
BMC Cell Biology
Mouse CCDC79 (TERB1) is a meiosis-specific telomere associated protein
Attila Tóth2  Manfred Alsheimer1  Yoshinori Watanabe3  Hiroki Shibuya3  Lukasz Wojtasz2  Daniel Tränkner2  Katrin Daniel2 
[1] Department of Cell and Developmental Biology, Biocenter, University of Würzburg, AmHubland, Würzburg 97074, Germany;Institute of Physiological Chemistry, Technische Universität Dresden, Fiedlerstr. 42, Dresden 01307, Germany;Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Tokyo 113-0032, Japan
关键词: SMC1B;    Meiotic cohesion;    Homologue pairing;    Recombination;    Nuclear envelope;    SUN1;    TERB1;    CCDC79;    Telomere attachment;    Telomeres;    Meiosis;   
Others  :  854525
DOI  :  10.1186/1471-2121-15-17
 received in 2013-12-06, accepted in 2014-05-14,  发布年份 2014
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【 摘 要 】

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.

【 授权许可】

   
2014 Daniel et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Gerton JL, Hawley RS: Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 2005, 6:477-487.
  • [2]Horn HF, Kim DI, Wright GD, Wong ES, Stewart CL, Burke B, Roux KJ: A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 2013, 202:1023-1039.
  • [3]Scherthan H: Telomere attachment and clustering during meiosis. Cell Mol Life Sci 2007, 64:117-124.
  • [4]Zickler D, Kleckner N: The leptotene-zygotene transition of meiosis. Annu Rev Genet 1998, 32:619-697.
  • [5]Hiraoka Y, Dernburg AF: The SUN rises on meiotic chromosome dynamics. Dev Cell 2009, 17:598-605.
  • [6]Harper L, Golubovskaya I, Cande WZ: A bouquet of chromosomes. J Cell Sci 2004, 117:4025-4032.
  • [7]Tomita K, Cooper JP: The telomere bouquet controls the meiotic spindle. Cell 2007, 130:113-126.
  • [8]Chikashige Y, Tsutsumi C, Yamane M, Okamasa K, Haraguchi T, Hiraoka Y: Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 2006, 125:59-69.
  • [9]Conrad MN, Lee CY, Wilkerson JL, Dresser ME: MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae Proc. Natl Acad Sci USA 2007, 104:8863-8868.
  • [10]Cooper JP, Watanabe Y, Nurse P: Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 1998, 392:828-831.
  • [11]Park MJ, Jang YK, Choi ES, Kim HS, Park SD: Fission yeast Rap1 homolog is a telomere-specific silencing factor and interacts with Taz1p. Mol Cells 2002, 13:327-333.
  • [12]Scherthan H, Sfeir A, de Lange T: Rap1-independent telomere attachment and bouquet formation in mammalian meiosis. Chromosoma 2011, 120:151-157.
  • [13]Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M: SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 2007, 12:863-872.
  • [14]Schmitt J, Benavente R, Hodzic D, Höög C, Stewart CL, Alsheimer M: Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc Natl Acad Sci USA 2007, 104:7426-7431.
  • [15]Link J, Jahn D, Leubner M, Schmitt J, Göb E, Benavente R, Jeang KT, Xu R, Alsheimer M: Analysis of meiosis in SUN1 deficient mice reveals a distinct role of SUN2 in mammalian meiotic LINC complex formation and function. PLoS Genetin press
  • [16]Siderakis M, Tarsounas M: Telomere regulation and function during meiosis. Chromosome Res 2007, 15:667-679.
  • [17]Liu D, O’Connor MS, Qin J, Songyang Z: Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J Biol Chem 2004, 279:51338-51342.
  • [18]Verdun RE, Karlseder J: Replication and protection of telomeres. Nature 2007, 447:924-931.
  • [19]Palm W, de Lange T: How shelterin protects mammalian telomeres. Annu Rev Genet 2008, 42:301-334.
  • [20]Adelfalk C, Janschek J, Revenkova E, Blei C, Liebe B, Göb E, Alsheimer M, Benavente R, de Boer E, Novak I, Höög C, Scherthan H, Jessberger R: Cohesin SMC1beta protects telomeres in meiocytes. J Cell Biol 2009, 187:185-199.
  • [21]Shibuya H, Ishiguro K, Watanabe Y: The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 2014, 16:145-156.
  • [22]Wojtasz L, Daniel K, Toth A: Fluorescence activated cell sorting of live female germ cells and somatic cells of the mouse fetal gonad based on forward and side scattering. Cytometry A 2009, 75:547-553.
  • [23]Aasland R, Stewart AF, Gibson T: The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. Trends Biochem Sci 1996, 3:87-88.
  • [24]Ogata K, Morikawa S, Nakamura H, Sekikawa A, Inoue T, Kanai H, Sarai A, Ishii S, Nishimura Y: Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell 1994, 79:639-648.
  • [25]König P, Giraldo R, Chapman L, Rhodes D: The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA. Cell 1996, 85:125-136.
  • [26]Cooper JP, Nimmo ER, Allshire RC, Cech TR: Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 1997, 385:744-747.
  • [27]Nishikawa T, Okamura H, Nagadoi A, König P, Rhodes D, Nishimura Y: Solution structure of a telomeric DNA complex of human TRF1. Structure 2001, 9:1237-1251.
  • [28]Yu EY, Kim SE, Kim JH, Ko JH, Cho MH, Chung IK: Sequence-specific DNA recognition by the Myb-like domain of plant telomeric protein RTBP1. J Biol Chem 2000, 275:24208-24214.
  • [29]Bilaud T, Koering CE, Binet-Brasselet E, Ancelin K, Pollice A, Gasser SM, Gilson E: The telobox, a Myb-related telomeric DNA binding motif found in proteins from yeast, plants and human. Nucleic Acids Res 1996, 24:1294-1303.
  • [30]Brun C, Marcand S, Gilson E: Proteins that bind to double-stranded regions of telomeric DNA. Trends Cell Biol 1997, 7:317-324.
  • [31]Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R: Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 2004, 6:555-562.
  • [32]Chi YH, Cheng LI, Myers T, Ward JM, Williams E, Su Q, Faucette L, Wang JY, Jeang KT: Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA. Development 2009, 136:965-973.
  • [33]Peters AH, Plug AW, van Vugt MJ, de Boer P: A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 1997, 5:66-68.
  • [34]Link J, Jahn D, Schmitt J, Göb E, Baar J, Ortega S, Benavente R, Alsheimer M: The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet 2013, 9(1):e1003261.
  • [35]Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C: Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 2003, 160:657-670.
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