LINC complexes as regulators of meiosis

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Meiosis is a key processes of sexual reproduction in eukaryotes. By combining two cell division cycles with a single round of DNA replication meiosis provides a mechanism to generate haploid gametes. Coincidentally, processes involved in ensuring appropriate segregation of homologous chromosomes also result in genetic recombination and shuffling of genes between each generation. During the first meiotic prophase, rapid telomere-led chromosome movements facilitate alignment and pairing of homologous chromosomes. Forces that produce these movements are generated by the cytoskeleton. Force transmission across the nuclear envelope is dependent upon LINC complexes. These structures consist of SUN and KASH domain proteins that span the two nuclear membranes. Together they represent a pair of links in a molecular chain that couples telomeres to the cytoskeleton. In addition to their force transducing role, LINC complexes also have essential functions ensuring the fidelity of recombination between homologous chromosomes. In this way, LINC complexes are now seen as playing an active and integral role in meiotic progression.

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Acknowledgements

This work was supported by the Agency for Science Technology and Research (A*STAR), Singapore. I am grateful to Dr. Lee Yin Loon for his helpful comments on the manuscript.

References (82)

  • D.A. Starr et al.

    Role of ANC-1 in tethering nuclei to the actin cytoskeleton

    Science

    (2002)
  • A. Woglar et al.

    Chromosome movement in meiosis I prophase of Caenorhabditis elegans

    Chromosoma

    (2013)
  • O. Rog et al.

    Direct visualization reveals kinetics of meiotic chromosome synapsis

    Cell Rep

    (2015)
  • D.J. Wynne et al.

    Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis

    J Cell Biol

    (2012)
  • C.M. Phillips et al.

    HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis

    Cell

    (2005)
  • A. Daryabeigi et al.

    Nuclear envelope retention of LINC complexes is promoted by SUN-1 oligomerization in the Caenorhabditis elegans germ line

    Genetics

    (2017)
  • F. Lottersberger et al.

    53BP1 and the LINC complex promote microtubule-dependent DSB mobility and DNA repair

    Cell

    (2015)
  • K. Lei et al.

    Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response

    Curr Biol

    (2012)
  • M. Jagut et al.

    Separable roles for a Caenorhabditis elegans RMI1 homolog in promoting and antagonizing meiotic crossovers ensure faithful chromosome inheritance

    PLoS Biol

    (2016)
  • K.S. Lawrence et al.

    LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining

    J Cell Biol

    (2016)
  • E. Pasch et al.

    The LINC complex component Sun4 plays a crucial role in sperm head formation and fertility

    Biol Open

    (2015)
  • C.-Y. Lee et al.

    Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes

    Cell Rep

    (2015)
  • A. Viera et al.

    CDK2 regulates nuclear envelope protein dynamics and telomere attachment in mouse meiotic prophase

    J Cell Sci

    (2015)
  • H. Shibuya et al.

    The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis

    Nat Cell Biol

    (2014)
  • X. Zhou et al.

    SUN anchors pollen WIP–WIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility

    J Exp Bot

    (2015)
  • H. Scherthan

    A bouquet makes ends meet

    Nat Rev Mol Cell Biol

    (2001)
  • K. Salonen et al.

    A colcemid-sensitive mechanism involved in regulation of chromosome movements during meiotic pairing

    Chromosoma

    (1982)
  • C.R. Bone et al.

    Nuclear migration events throughout development

    J Cell Sci

    (2016)
  • K.L. Wilson et al.

    Evolution: functional evolution of nuclear structure

    J Cell Biol

    (2011)
  • B. Burke et al.

    The nuclear lamins: flexibility in function

    Nat Rev Mol Cell Biol

    (2013)
  • Y. Chikashige et al.

    Telomere-led premeiotic chromosome movement in fission yeast

    Science

    (1994)
  • D.Q. Ding et al.

    Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells

    J Cell Sci

    (1998)
  • M. Shimanuki et al.

    A novel fission yeast gene, kms1+, is required for the formation of meiotic prophase-specific nuclear architecture

    Mol Gen Genet

    (1997)
  • Y. Chikashige et al.

    Membrane proteins Bqt3 and -4 anchor telomeres to the nuclear envelope to ensure chromosomal bouquet formation

    J Cell Biol

    (2009)
  • S. Gudise et al.

    Samp1 is functionally associated with the LINC complex and A-type lamina networks

    J Cell Sci

    (2011)
  • A. Fernández-Álvarez et al.

    The functionally elusive RabI chromosome configuration directly regulates nuclear membrane remodeling at mitotic onset

    Cell Cycle

    (2017)
  • M. Klutstein et al.

    The telomere bouquet regulates meiotic centromere assembly

    Nat Cell Biol

    (2015)
  • M.N. Conrad et al.

    Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination

    Cell

    (2008)
  • E. Trelles-Sticken et al.

    Meiotic telomere clustering requires actin for its formation and cohesin for its resolution

    J Cell Biol

    (2005)
  • S.L. Jaspersen et al.

    Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p

    J Cell Biol

    (2002)
  • M.N. Conrad et al.

    MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae

    Proc Natl Acad Sci USA

    (2007)
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