Pairing of homologous chromosomes in C. elegans meiosis requires DEB-1 - an orthologue of mammalian vinculin

. 2019 Dec ; 10 (1) : 93-115.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31068058

During meiosis, homologous chromosomes undergo a dramatic movement in order to correctly align. This is a critical meiotic event but the molecular properties of this 'chromosomal dance' still remainunclear. We identified DEB-1 - an orthologue of mammalian vinculin - as a new component of the mechanistic modules responsible for attaching the chromosomes to the nuclear envelope as apart of the LINC complex. In early meiotic nuclei of C. elegans, DEB-1 is localized to the nuclear periphery and alongside the synaptonemal complex of paired homologues. Upon DEB-1 depletion, chromosomes attached to SUN-1 foci remain highly motile until late pachytene. Although the initiation of homologue pairing started normally, irregularities in the formation of the synaptonemal complex occur, and these results in meiotic defects such as increased number of univalents at diakinesis and high embryonic lethality. Our data identify DEB-1 as a new player regulating chromosome dynamics and pairing during meiotic prophase I.

Zobrazit více v PubMed

Page SL, Hawley RS.. The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol. 2004;20:525–558. PubMed

MacQueen AJ, Phillips CM, Bhalla N, et al. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell. 2005;123(6):1037–1050. PubMed PMC

Sato A, Isaac B, Phillips CM, et al. Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell. 2009;139(5):907–919. PubMed PMC

Penkner A, Tang L, Novatchkova M, et al. The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell. 2007;12(6):873–885. PubMed

Hayashi M, Mlynarczyk-Evans S, Villeneuve AM. The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics. 2010;186(1):45–58. PubMed PMC

Phillips CM, Wong C, Bhalla N, et al. HIM–8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell. 2005;123:1051–1063. PubMed PMC

Phillips CM, Dernburg AF. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell. 2006;11:817–829. PubMed

Woglar A, Jantsch V. Chromosome movement in meiosis I prophase of Caenorhabditis elegans. Chromosoma. 2014;123(1–2):15–24. PubMed PMC

Wynne DJ, Rog O, Carlton PM, et al. Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis. J Cell Biol. 2012;196(1):47–64. PubMed PMC

Hirsh D, Oppenheim D, Klass M. Development of the reproductive system of Caenorhabditis elegans. Dev Biol. 1976;49(1):200–219. PubMed

Bakolitsa C, Cohen DM, Bankston LA, et al. Structural basis for vinculin activation at sites of cell adhesion. Nature. 2004;430(6999):583–586. PubMed

Winkler J, Lunsdorf H, Jockusch BM. The ultrastructure of chicken gizzard vinculin as visualized by high-resolution electron microscopy. J Struct Biol. 1996;116(2):270–277. PubMed

Geiger B, Volk T, Volberg T. Molecular heterogeneity of adherens junctions. J Cell Biol. 1985;101(4):1523–1531. PubMed PMC

Koteliansky VE, Gneushev GN. Vinculin localization in cardiac muscle. FEBS Lett. 1983;159(1–2):158–160. PubMed

Terracio L, Simpson DG, Hilenski L, et al. Distribution of vinculin in the Z-disk of striated muscle: analysis by laser scanning confocal microscopy. J Cell Physiol. 1990;145(1):78–87. PubMed

Samarel AM. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol. 2005;289(6):H2291–301. PubMed

Peng X, Nelson ES, Maiers JL, et al. New insights into vinculin function and regulation. Int Rev Cell Mol Biol. 2011;287:191–231. PubMed PMC

Barstead RJ, Waterston RH. The basal component of the nematode dense-body is vinculin. J Biol Chem. 1989;264(17):10177–10185. PubMed

Rogalski TM, Mullen GP, Gilbert MM, et al. The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol. 2000;150(1):253–264. PubMed PMC

Francis GR, Waterston RH. Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol. 1985;101(4):1532–1549. PubMed PMC

Ono K, Yu R, Ono S. Structural components of the nonstriated contractile apparatuses in the Caenorhabditis elegans gonadal myoepithelial sheath and their essential roles for ovulation. Dev Dyn. 2007;236(4):1093–1105. PubMed PMC

Iwasaki K, McCarter J, Francis R, et al. emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. J Cell Biol. 1996;134(3):699–714. PubMed PMC

McCarter J, Bartlett B, Dang T, et al. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol. 1999;205(1):111–128. PubMed

McCarter J, Bartlett B, Dang T, et al. Soma-germ cell interactions in Caenorhabditis elegans: multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineages. Dev Biol. 1997;181(2):121–143. PubMed

Williams BD, Waterston RH. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol. 1994;124(4):475–490. PubMed PMC

Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974;77(1):71–94. PubMed PMC

Timmons L, Fire A. Specific interference by ingested dsRNA. Nature. 1998;395(6705):854. PubMed

Martinez-Perez E, Villeneuve AM. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19(22):2727–2743. PubMed PMC

MacQueen AJ, Colaiácovo MP, McDonald K, et al. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–2442. PubMed PMC

Penkner AM, Fridkin A, Gloggnitzer J, et al. Meiotic chromosome homology search involves modifications of the nuclear envelope protein Matefin/SUN-1. Cell. 2009;139(5):920–933. PubMed

Labella S, Woglar A, Jantsch V, et al. Polo kinases establish links between meiotic chromosomes and cytoskeletal forces essential for homolog pairing. Dev Cell. 2011;21(5):948–958. PubMed

Matsuura R, Ashikawa T, Nozaki Y, et al. LIN-41 inactivation leads to delayed centrosome elimination and abnormal chromosome behavior during female meiosis in Caenorhabditis elegans. Mol Biol Cell. 2016;27(5):799–811. PubMed PMC

MacQueen AJ, Villeneuve AM. Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 2001;15(13):1674–1687. PubMed PMC

Dernburg AF, McDonald K, Moulder G, et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell. 1998;94(3):387–398. PubMed

Philimonenko AA, Janacek J, Hozak P. Statistical evaluation of colocalization patterns in immunogold labeling experiments. J Struct Biol. 2000;132(3):201–210. PubMed

Barstead RJ, Waterston RH. Vinculin is essential for muscle function in the nematode. J Cell Biol. 1991;114(4):715–724. PubMed PMC

Kumsta C, Hansen M. C. elegans rrf-1 mutations maintain RNAi efficiency in the soma in addition to the germline. PLoS One. 2012;7(5):e35428. PubMed PMC

Kalocsay M, Hiller NJ, Jentsch S. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell. 2009;33(3):335–343. PubMed

Cohen TV, Stewart CL. Fraying at the edge mouse models of diseases resulting from defects at the nuclear periphery. Curr Top Dev Biol. 2008;84:351–384. PubMed

Dahl KN, Engler AJ, Pajerowski JD, et al. Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys J. 2005;89(4):2855–2864. PubMed PMC

Jaalouk DE, Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol. 2009;10(1):63–73. PubMed PMC

Janmey PA, McCulloch CA. Cell mechanics: integrating cell responses to mechanical stimuli. Annu Rev Biomed Eng. 2007;9:1–34. PubMed

Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol. 2009;10(1):75–82. PubMed

Conrad MN, Lee C-Y, Wilkerson JL, et al. MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2007;104(21):8863–8868. PubMed PMC

Lin X, Qadota H, Moerman DG, et al. C. elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr Biol. 2003;13(11):922–932. PubMed

Ding X, Xu R, Yu J, et al. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell. 2007;12(6):863–872. PubMed

Daryabeigi A, Woglar A, Baudrimont A, et al. Nuclear envelope retention of LINC complexes is promoted by SUN-1 oligomerization in the caenorhabditis elegans germ line. Genetics. 2016;203(2):733–748. PubMed PMC

Goodyer W, Kaitna S, Couteau F, et al. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell. 2008;14(2):263–274. PubMed

Colaiácovo MP, MacQueen AJ, Martinez-Perez E, et al. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell. 2003;5(3):463–474. PubMed

Couteau F, Nabeshima K, Villeneuve A, et al. A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol. 2004;14(7):585–592. PubMed

Yokoo R, Zawadzki KA, Nabeshima K, et al. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012;149(1):75–87. PubMed PMC

Chang W, Worman HJ, Gundersen GG. Accessorizing and anchoring the LINC complex for multifunctionality. J Cell Biol. 2015;208(1):11–22. PubMed PMC

Koszul R, Kleckner N. Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol. 2009;19(12):716–724. PubMed PMC

Kaverina I, Rottner K, Small JV. Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol. 1998;142(1):181–190. PubMed PMC

Rodriguez OC, Schaefer AW, Mandato CA, et al. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol. 2003;5(7):599–609. PubMed

Schober JM, Kwon G, Jayne D, et al. The microtubule-associated protein EB1 maintains cell polarity through activation of protein kinase C. Biochem Biophys Res Commun. 2012;417(1):67–72. PubMed PMC

Gerton JL, Hawley RS. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet. 2005;6(6):477–487. PubMed

Bhalla N, Dernburg AF. Prelude to a division. Annu Rev Cell Dev Biol. 2008;24:397–424. PubMed PMC

Bozza CG, Pawlowski WP. The cytogenetics of homologous chromosome pairing in meiosis in plants. Cytogenet Genome Res. 2008;120(3–4):313–319. PubMed

Stewart MN, Dawson DS. Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet. 2008;24(11):564–573. PubMed PMC

Loidl J. The initiation of meiotic chromosome pairing: the cytological view. Genome. 1990;33(6):759–778. PubMed

Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. PubMed

Nabeshima K. Collaborative homologous pairing during C. elegans meiosis. Worm. 2012;1(2):116–120. PubMed PMC

Tsai JH, McKee BD. Homologous pairing and the role of pairing centers in meiosis. J Cell Sci. 2011;124(Pt 12):1955–1963. PubMed

Ziegler WH, Liddington RC, Critchley DR. The structure and regulation of vinculin. Trends Cell Biol. 2006;16(9):453–460. PubMed

Chen H, Cohen DM, Choudhury DM, et al. Spatial distribution and functional significance of activated vinculin in living cells. J Cell Biol. 2005;169(3):459–470. PubMed PMC

Izard T, Vonrhein C. Structural basis for amplifying vinculin activation by talin. J Biol Chem. 2004;279(26):27667–27678. PubMed

Izard T, Evans G, Borgon RA, et al. Vinculin activation by talin through helical bundle conversion. Nature. 2004;427(6970):171–175. PubMed

Chorev DS, Volberg T, Livne A, et al. Conformational states during vinculin unlocking differentially regulate focal adhesion properties. Sci Rep. 2018;8(1):2693. PubMed PMC

Balaban NQ, Schwarz US, Riveline D, et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol. 2001;3(5):466–472. PubMed

Hiraoka Y, Dernburg AF. The SUN rises on meiotic chromosome dynamics. Dev Cell. 2009;17(5):598–605. PubMed

Harper NC, Rillo R, Jover-Gil S, et al. Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell. 2011;21(5):934–947. PubMed PMC

Fridkin A, Mills E, Margalit A, et al. Matefin, a Caenorhabditis elegans germ line-specific SUN-domain nuclear membrane protein, is essential for early embryonic and germ cell development. Proc Natl Acad Sci U S A. 2004;101(18):6987–6992. PubMed PMC

Jaspersen SL, Hawley RS. Meiotic pairing as a polo match. Dev Cell. 2011;21(5):805–806. PubMed

Hieda M. Implications for diverse functions of the LINC complexes based on the structure. Cells. 2017;6:3. PubMed PMC

Janin A, Bauer D, Ratti F, et al. Nuclear envelopathies: a complex LINC between nuclear envelope and pathology. Orphanet J Rare Dis. 2017;12(1):147. PubMed PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...