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Structural basis of meiotic telomere attachment to the nuclear envelope by MAJIN-TERB2-TERB1.

Dunce JM, Milburn AE, Gurusaran M, da Cruz I, Sen LT, Benavente R, Davies OR
Nat Commun 9 5355 (2018)
Cited: 23 times
EuropePMC logo PMID: 30559341

Abstract

Meiotic chromosomes undergo rapid prophase movements, which are thought to facilitate the formation of inter-homologue recombination intermediates that underlie synapsis, crossing over and segregation. The meiotic telomere complex (MAJIN, TERB1, TERB2) tethers telomere ends to the nuclear envelope and transmits cytoskeletal forces via the LINC complex to drive these rapid movements. Here, we report the molecular architecture of the meiotic telomere complex through the crystal structure of MAJIN-TERB2, together with light and X-ray scattering studies of wider complexes. The MAJIN-TERB2 2:2 hetero-tetramer binds strongly to DNA and is tethered through long flexible linkers to the inner nuclear membrane and two TRF1-binding 1:1 TERB2-TERB1 complexes. Our complementary structured illumination microscopy studies and biochemical findings reveal a telomere attachment mechanism in which MAJIN-TERB2-TERB1 recruits telomere-bound TRF1, which is then displaced during pachytene, allowing MAJIN-TERB2-TERB1 to bind telomeric DNA and form a mature attachment plate.

Articles - 6gnx mentioned but not cited (5)

  1. Structural basis of meiotic telomere attachment to the nuclear envelope by MAJIN-TERB2-TERB1. Dunce JM, Milburn AE, Gurusaran M, da Cruz I, Sen LT, Benavente R, Davies OR. Nat Commun 9 5355 (2018)
  2. Analyzing effect of quadruple multiple sequence alignments on deep learning based protein inter-residue distance prediction. Jain A, Terashi G, Kagaya Y, Maddhuri Venkata Subramaniya SR, Christoffer C, Kihara D. Sci Rep 11 7574 (2021)
  3. Small angle X-ray scattering-assisted protein structure prediction in CASP13 and emergence of solution structure differences. Hura GL, Hodge CD, Rosenberg D, Guzenko D, Duarte JM, Monastyrskyy B, Grudinin S, Kryshtafovych A, Tainer JA, Fidelis K, Tsutakawa SE. Proteins 87 1298-1314 (2019)
  4. Target highlights in CASP13: Experimental target structures through the eyes of their authors. Lepore R, Kryshtafovych A, Alahuhta M, Veraszto HA, Bomble YJ, Bufton JC, Bullock AN, Caba C, Cao H, Davies OR, Desfosses A, Dunne M, Fidelis K, Goulding CW, Gurusaran M, Gutsche I, Harding CJ, Hartmann MD, Hayes CS, Joachimiak A, Leiman PG, Loppnau P, Lovering AL, Lunin VV, Michalska K, Mir-Sanchis I, Mitra AK, Moult J, Phillips GN, Pinkas DM, Rice PA, Tong Y, Topf M, Walton JD, Schwede T. Proteins 87 1037-1057 (2019)
  5. Simultaneous Assignment and Structure Determination of Proteins From Sparsely Labeled NMR Datasets. Mondal A, Perez A. Front Mol Biosci 8 774394 (2021)


Reviews citing this publication (3)

  1. Crossover Interference: Shedding Light on the Evolution of Recombination. Otto SP, Payseur BA. Annu Rev Genet 53 19-44 (2019)
  2. Diverse roles for CDK-associated activity during spermatogenesis. Palmer N, Talib SZA, Kaldis P. FEBS Lett. 593 2925-2949 (2019)
  3. Meiotic Chromosome Dynamics in Zebrafish. Imai Y, Olaya I, Sakai N, Burgess SM. Front Cell Dev Biol 9 757445 (2021)

Articles citing this publication (15)

  1. Tethering of Telomeres to the Nuclear Envelope Is Mediated by SUN1-MAJIN and Possibly Promoted by SPDYA-CDK2 During Meiosis. Wang G, Wu X, Zhou L, Gao S, Yun D, Liang A, Sun F. Front Cell Dev Biol 8 845 (2020)
  2. Homozygous missense mutation in CCDC155 disrupts the transmembrane distribution of CCDC155 and SUN1, resulting in non-obstructive azoospermia and premature ovarian insufficiency in humans. Wu H, Zhang X, Hua R, Li Y, Cheng L, Li K, Liu Y, Gao Y, Shen Q, Wang G, Lv M, Xu Y, He X, Cao Y, Liu M. Hum Genet 141 1795-1809 (2022)
  3. Meiotic chromosomes in motion: a perspective from Mus musculus and Caenorhabditis elegans. Link J, Jantsch V. Chromosoma 128 317-330 (2019)
  4. Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment. Zuo W, Chen G, Gao Z, Li S, Chen Y, Huang C, Chen J, Chen Z, Lei M, Bian Q. Nat Commun 12 5827 (2021)
  5. The meiotic TERB1-TERB2-MAJIN complex tethers telomeres to the nuclear envelope. Wang Y, Chen Y, Chen J, Wang L, Nie L, Long J, Chang H, Wu J, Huang C, Lei M. Nat Commun 10 564 (2019)
  6. Meiotic behavior, transmission and active genes of B chromosomes in the cichlid Astatotilapia latifasciata: new clues about nature, evolution and maintenance of accessory elements. Cardoso AL, Venturelli NB, da Cruz I, de Sá Patroni FM, de Moraes D, de Oliveira RA, Benavente R, Martins C. Mol Genet Genomics 297 1151-1167 (2022)
  7. The SUN1-SPDYA interaction plays an essential role in meiosis prophase I. Chen Y, Wang Y, Chen J, Zuo W, Fan Y, Huang S, Liu Y, Chen G, Li Q, Li J, Wu J, Bian Q, Huang C, Lei M. Nat Commun 12 3176 (2021)
  8. The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans. da Cruz I, Brochier-Armanet C, Benavente R. BMC Evol Biol 20 55 (2020)
  9. Brain resilience across the general cognitive ability distribution: Evidence from structural connectivity. Santonja J, Martínez K, Román FJ, Escorial S, Quiroga MÁ, Álvarez-Linera J, Iturria-Medina Y, Santarnecchi E, Colom R. Brain Struct Funct (2021)
  10. Computational Analysis of the Potential Impact of MTC Complex Missenses SNPs Associated with Male Infertility. Harmak H, Charoute H, Redouane S, Filali OA, Barakat A, Rouba H. Biomed Res Int 2022 1664825 (2022)
  11. Disruption of human meiotic telomere complex genes TERB1, TERB2 and MAJIN in men with non-obstructive azoospermia. Salas-Huetos A, Tüttelmann F, Wyrwoll MJ, Kliesch S, Lopes AM, Goncalves J, Boyden SE, Wöste M, Hotaling JM, GEMINI Consortium, Nagirnaja L, Conrad DF, Carrell DT, Aston KI. Hum Genet 140 217-227 (2021)
  12. Kinetic analysis of synaptonemal complex dynamics during meiosis of yeast Saccharomyces cerevisiae reveals biphasic growth and abortive disassembly. Pollard MG, Rockmill B, Oke A, Anderson CM, Fung JC. Front Cell Dev Biol 11 1098468 (2023)
  13. Molecular insights into LINC complex architecture through the crystal structure of a luminal trimeric coiled-coil domain of SUN1. Gurusaran M, Biemans JJ, Wood CW, Davies OR. Front Cell Dev Biol 11 1144277 (2023)
  14. The TERB1 MYB domain suppresses telomere erosion in meiotic prophase I. Zhang K, Tarczykowska A, Gupta DK, Pendlebury DF, Zuckerman C, Nandakumar J, Shibuya H. Cell Rep 38 110289 (2022)
  15. The meiotic LINC complex component KASH5 is an activating adaptor for cytoplasmic dynein. Garner KEL, Salter A, Lau CK, Gurusaran M, Villemant CM, Granger EP, McNee G, Woodman PG, Davies OR, Burke BE, Allan VJ. J Cell Biol 222 e202204042 (2023)


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