Literature DB >> 19913287

Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis.

Aya Sato1, Berith Isaac, Carolyn M Phillips, Regina Rillo, Peter M Carlton, David J Wynne, Roshni A Kasad, Abby F Dernburg.   

Abstract

During meiosis, each chromosome must pair with its unique homologous partner, a process that usually culminates with the formation of the synaptonemal complex (SC). In the nematode Caenorhabditis elegans, special regions on each chromosome known as pairing centers are essential for both homologous pairing and synapsis. We report that during early meiosis, pairing centers establish transient connections to the cytoplasmic microtubule network. These connections through the intact nuclear envelope require the SUN/KASH domain protein pair SUN-1 and ZYG-12. Disruption of microtubules inhibits chromosome pairing, indicating that these connections promote interhomolog interactions. Dynein activity is essential to license formation of the SC once pairing has been accomplished, most likely by overcoming a barrier imposed by the chromosome-nuclear envelope connection. Our findings thus provide insight into how homolog pairing is accomplished in meiosis and into the mechanisms regulating synapsis so that it occurs selectively between homologs. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.

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Year:  2009        PMID: 19913287      PMCID: PMC2825574          DOI: 10.1016/j.cell.2009.10.039

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  46 in total

1.  Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis.

Authors:  O Niwa; M Shimanuki; F Miki
Journal:  EMBO J       Date:  2000-07-17       Impact factor: 11.598

2.  Functional genomic analysis of C. elegans chromosome I by systematic RNA interference.

Authors:  A G Fraser; R S Kamath; P Zipperlen; M Martinez-Campos; M Sohrmann; J Ahringer
Journal:  Nature       Date:  2000-11-16       Impact factor: 49.962

3.  Reorganization and polarization of the meiotic bouquet-stage cell can be uncoupled from telomere clustering.

Authors:  Carrie R Cowan; Peter M Carlton; W Zacheus Cande
Journal:  J Cell Sci       Date:  2002-10-01       Impact factor: 5.285

4.  Probing the interaction of HTI-286 with tubulin using a stilbene analogue.

Authors:  Mei-Chu Lo; Ann Aulabaugh; Girija Krishnamurthy; Joshua Kaplan; Arie Zask; Robert P Smith; George Ellestad
Journal:  J Am Chem Soc       Date:  2004-08-18       Impact factor: 15.419

Review 5.  Telomere attachment and clustering during meiosis.

Authors:  H Scherthan
Journal:  Cell Mol Life Sci       Date:  2007-01       Impact factor: 9.261

6.  Telomere-led premeiotic chromosome movement in fission yeast.

Authors:  Y Chikashige; D Q Ding; H Funabiki; T Haraguchi; S Mashiko; M Yanagida; Y Hiraoka
Journal:  Science       Date:  1994-04-08       Impact factor: 47.728

7.  Colchicine effects on meiosis in the male mouse. I. Meiotic prophase: synaptic arrest, univalents, loss of damaged spermatocytes and a possible checkpoint at pachytene.

Authors:  J H Tepperberg; M J Moses; J Nath
Journal:  Chromosoma       Date:  1997-08       Impact factor: 4.316

8.  Chromosome-wide control of meiotic crossing over in C. elegans.

Authors:  Kenneth J Hillers; Anne M Villeneuve
Journal:  Curr Biol       Date:  2003-09-16       Impact factor: 10.834

9.  Dynein modifiers in C. elegans: light chains suppress conditional heavy chain mutants.

Authors:  Sean M O'Rourke; Marc D Dorfman; J Clayton Carter; Bruce Bowerman
Journal:  PLoS Genet       Date:  2007-08       Impact factor: 5.917

10.  Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination.

Authors:  Hiromichi Kosaka; Miki Shinohara; Akira Shinohara
Journal:  PLoS Genet       Date:  2008-09-26       Impact factor: 5.917

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  148 in total

1.  Rap1-independent telomere attachment and bouquet formation in mammalian meiosis.

Authors:  Harry Scherthan; Agnel Sfeir; Titia de Lange
Journal:  Chromosoma       Date:  2010-10-07       Impact factor: 4.316

2.  The nuclear envelope at a glance.

Authors:  Katherine L Wilson; Jason M Berk
Journal:  J Cell Sci       Date:  2010-06-15       Impact factor: 5.285

3.  Broad chromosomal domains of histone modification patterns in C. elegans.

Authors:  Tao Liu; Andreas Rechtsteiner; Thea A Egelhofer; Anne Vielle; Isabel Latorre; Ming-Sin Cheung; Sevinc Ercan; Kohta Ikegami; Morten Jensen; Paulina Kolasinska-Zwierz; Heidi Rosenbaum; Hyunjin Shin; Scott Taing; Teruaki Takasaki; A Leonardo Iniguez; Arshad Desai; Abby F Dernburg; Hiroshi Kimura; Jason D Lieb; Julie Ahringer; Susan Strome; X Shirley Liu
Journal:  Genome Res       Date:  2010-12-22       Impact factor: 9.043

Review 4.  Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges.

Authors:  Daniel A Starr; Heidi N Fridolfsson
Journal:  Annu Rev Cell Dev Biol       Date:  2010       Impact factor: 13.827

Review 5.  Making the LINC: SUN and KASH protein interactions.

Authors:  Dae In Kim; K C Birendra; Kyle J Roux
Journal:  Biol Chem       Date:  2015-04       Impact factor: 3.915

Review 6.  Geometry and force behind kinetochore orientation: lessons from meiosis.

Authors:  Yoshinori Watanabe
Journal:  Nat Rev Mol Cell Biol       Date:  2012-05-16       Impact factor: 94.444

Review 7.  Cell Biology of the Caenorhabditis elegans Nucleus.

Authors:  Orna Cohen-Fix; Peter Askjaer
Journal:  Genetics       Date:  2017-01       Impact factor: 4.562

8.  Bi-directional transport of the nucleus by dynein and kinesin-1.

Authors:  Marvin E Tanenbaum; Anna Akhmanova; René H Medema
Journal:  Commun Integr Biol       Date:  2011-01

9.  Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution.

Authors:  Thomas Cavalier-Smith
Journal:  Biol Direct       Date:  2010-02-04       Impact factor: 4.540

Review 10.  Genetics of mammalian meiosis: regulation, dynamics and impact on fertility.

Authors:  Mary Ann Handel; John C Schimenti
Journal:  Nat Rev Genet       Date:  2010-01-06       Impact factor: 53.242

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