A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization
Abstract
:1. Background
2. Results
2.1. Nanoscale Chromatin Compaction Is Decreased in Set-2 Mutant Germlines
2.2. Loss of Set-2 Enhances Defects in Germline Chromatin Organization Resulting from Condensin-II Knock-Down
2.3. Loss of Set-2 Differentially Affects Germline and Somatic Phenotypes of the Condensin-II Mutant Hcp-6(mr17)
2.4. Functional Links between SET-2 and Chromosome Structural Protein TOP-2 in Germline Organization
2.5. Set-2 Inactivation Does Not Affect Germline Expression of Condensins, Topoisomerase, or Other Genes with a Known Role in Chromosome Structure or Segregation
2.6. Loss of COMPASS Targeting Subunit CFP-1 Results in Similar Chromatin Organization Defects as Loss of SET-2
3. Discussion
4. Conclusions
5. Methods
5.1. Nematode Maintenance and Strains
5.2. Worm Preparation for Live-Imaging
5.3. FLIM-FRET Data Acquisition
5.4. FLIM-FRET Analysis
5.5. Condensin RNAi Knockdown
5.6. RNA Isolation and qRT-PCR Analysis
5.7. Hoechst Staining on Dissected Germlines
5.8. DAPI Staining on Whole Animals
5.9. Scoring of Germline Phenotypes
5.10. Sequencing and Mapping of the Hcp-6(mr17) Mutation
5.11. Brood Size and Embryonic Lethality Assays
5.12. Visualization of Apoptotic Cells in the Germline
5.13. RNA Sequencing of Dissected Gonads
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Rowley, M.J.; Corces, V.G. Organizational principles of 3D genome architecture. Nat. Rev. Genet. 2018, 19, 789–800. [Google Scholar] [CrossRef]
- Antonin, W.; Neumann, H. Chromosome condensation and decondensation during mitosis. Curr. Opin. Cell Biol. 2016, 40, 15–22. [Google Scholar] [CrossRef] [Green Version]
- Borde, V.; Robine, N.; Lin, W.; Bonfils, S.; Geli, V.; Nicolas, A. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 2009, 28, 99–111. [Google Scholar] [CrossRef] [Green Version]
- Buard, J.; Barthès, P.; Grey, C.; de Massy, B. Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J. 2009, 28, 2616–2624. [Google Scholar] [CrossRef] [Green Version]
- Lam, K.-W.G.; Brick, K.; Cheng, G.; Pratto, F.; Camerini-Otero, R.D. Cell-type-specific genomics reveals histone modification dynamics in mammalian meiosis. Nat. Commun. 2019, 10, 3821. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eissenberg, J.C.; Shilatifard, A. Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev. Biol. 2010, 339, 240–249. [Google Scholar] [CrossRef] [Green Version]
- Dehe, P.M.; Dichtl, B.; Schaft, D.; Roguev, A.; Pamblanco, M.; Lebrun, R.; Rodriguez-Gil, A.; Mkandawire, M.; Landsberg, K.; Shevchenko, A.; et al. Protein interactions within the Set1 complex and their roles in the regulation of histone 3 lysine 4 methylation. J. Biol. Chem. 2006, 281, 35404–35412. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Howe, F.S.; Fischl, H.; Murray, S.C.; Mellor, J. Is H3K4me3 instructive for transcription activation? BioEssays News Rev. Mol. Cell. Dev. Biol. 2017, 39, 1–12. [Google Scholar] [CrossRef]
- Acquaviva, L.; Szekvolgyi, L.; Dichtl, B.; Dichtl, B.S.; de la Roche-Saint-Andre, C.; Nicolas, A.; Geli, V. The COMPASS subunit Spp1 links histone methylation to initiation of meiotic recombination. Science 2013, 339, 215–218. [Google Scholar] [CrossRef] [PubMed]
- Sommermeyer, V.; Beneut, C.; Chaplais, E.; Serrentino, M.E.; Borde, V. Spp1, a member of the Set1 Complex, promotes meiotic DSB formation in promoters by tethering histone H3K4 methylation sites to chromosome axes. Mol. Cell 2013, 49, 43–54. [Google Scholar] [CrossRef] [Green Version]
- Adam, C.; Guérois, R.; Citarella, A.; Verardi, L.; Adolphe, F.; Béneut, C.; Sommermeyer, V.; Ramus, C.; Govin, J.; Couté, Y.; et al. The PHD finger protein Spp1 has distinct functions in the Set1 and the meiotic DSB formation complexes. PLoS Genet. 2018, 14, e1007223. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mikheyeva, I.V.; Grady, P.J.R.; Tamburini, F.B.; Lorenz, D.R.; Cam, H.P. Multifaceted genome control by Set1 Dependent and Independent of H3K4 methylation and the Set1C/COMPASS complex. PLoS Genet. 2014, 10, e1004740. [Google Scholar] [CrossRef] [PubMed]
- Lorenz, D.R.; Mikheyeva, I.V.; Johansen, P.; Meyer, L.; Berg, A.; Grewal, S.I.S.; Cam, H.P. CENP-B cooperates with Set1 in bidirectional transcriptional silencing and genome organization of retrotransposons. Mol. Cell. Biol. 2012, 32, 4215–4225. [Google Scholar] [CrossRef] [Green Version]
- Sha, Q.-Q.; Dai, X.-X.; Jiang, J.-C.; Yu, C.; Jiang, Y.; Liu, J.; Ou, X.-H.; Zhang, S.-Y.; Fan, H.-Y. CFP1 coordinates histone H3 lysine-4 trimethylation and meiotic cell cycle progression in mouse oocytes. Nat. Commun. 2018, 9, 3477. [Google Scholar] [CrossRef] [PubMed]
- Herbette, M.; Mercier, M.G.; Michal, F.; Cluet, D.; Burny, C.; Yvert, G.; Robert, V.J.; Palladino, F. The C. elegans SET-2/SET1 histone H3 Lys4 (H3K4) methyltransferase preserves genome stability in the germline. DNA Repair 2017, 57, 139–150. [Google Scholar] [CrossRef]
- Li, T.; Kelly, W.G. A role for Set1/MLL-related components in epigenetic regulation of the Caenorhabditis elegans germ line. PLoS Genet. 2011, 7, e1001349. [Google Scholar] [CrossRef] [Green Version]
- Robert, V.J.; Mercier, M.G.; Bedet, C.; Janczarski, S.; Merlet, J.; Garvis, S.; Ciosk, R.; Palladino, F. The SET-2/SET1 histone H3K4 methyltransferase maintains pluripotency in the Caenorhabditis elegans germline. Cell Rep. 2014, 9, 443–450. [Google Scholar] [CrossRef] [Green Version]
- Xiao, Y.; Bedet, C.; Robert, V.J.; Simonet, T.; Dunkelbarger, S.; Rakotomalala, C.; Soete, G.; Korswagen, H.C.; Strome, S.; Palladino, F. Caenorhabditis elegans chromatin-associated proteins SET-2 and ASH-2 are differentially required for histone H3 Lys 4 methylation in embryos and adult germ cells. Proc. Natl. Acad. Sci. USA 2011, 108, 8305–8310. [Google Scholar] [CrossRef] [Green Version]
- Beurton, F.; Stempor, P.; Caron, M.; Appert, A.; Dong, Y.; Chen, R.A.-J.; Cluet, D.; Couté, Y.; Herbette, M.; Huang, N.; et al. Physical and functional interaction between SET1/COMPASS complex component CFP-1 and a Sin3S HDAC complex in C. elegans. Nucleic Acids Res. 2019. [Google Scholar] [CrossRef] [Green Version]
- Clouaire, T.; Webb, S.; Skene, P.; Illingworth, R.; Kerr, A.; Andrews, R.; Lee, J.-H.; Skalnik, D.; Bird, A. Cfp1 integrates both CpG content and gene activity for accurate H3K4me3 deposition in embryonic stem cells. Genes Dev. 2012, 26, 1714–1728. [Google Scholar] [CrossRef] [Green Version]
- Clouaire, T.; Webb, S.; Bird, A. Cfp1 is required for gene expression-dependent H3K4 trimethylation and H3K9 acetylation in embryonic stem cells. Genome Biol. 2014, 15, 451. [Google Scholar] [CrossRef] [PubMed]
- Lenstra, T.L.; Benschop, J.J.; Kim, T.; Schulze, J.M.; Brabers, N.A.; Margaritis, T.; van de Pasch, L.A.; van Heesch, S.A.; Brok, M.O.; Groot-Koerkamp, M.J.; et al. The specificity and topology of chromatin interaction pathways in yeast. Mol. Cell 2011, 42, 536–549. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weiner, A.; Chen, H.V.; Liu, C.L.; Rahat, A.; Klien, A.; Soares, L.; Gudipati, M.; Pfeffner, J.; Regev, A.; Buratowski, S.; et al. Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol. 2012, 10, e1001369. [Google Scholar] [CrossRef] [Green Version]
- Hirano, T. Condensins: Universal organizers of chromosomes with diverse functions. Genes Dev. 2012, 26, 1659–1678. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adachi, Y.; Luke, M.; Laemmli, U.K. Chromosome assembly in vitro: Topoisomerase II is required for condensation. Cell 1991, 64, 137–148. [Google Scholar] [CrossRef]
- Hirano, T.; Mitchison, T.J. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J. Cell Biol. 1993, 120, 601–612. [Google Scholar] [CrossRef]
- Uemura, T.; Ohkura, H.; Adachi, Y.; Morino, K.; Shiozaki, K.; Yanagida, M. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 1987, 50, 917–925. [Google Scholar] [CrossRef]
- Kimble, J.; Crittenden, S.L. Germline proliferation and its control. In WormBook: The Online Review of C. elegans Biology; WormBook: Pasadena, CA, USA, 2005; pp. 1–14. [Google Scholar] [CrossRef]
- Fisher, K.; Southall, S.M.; Wilson, J.R.; Poulin, G.B. Methylation and demethylation activities of a C. elegans MLL-like complex attenuate RAS signalling. Dev. Biol. 2010, 341, 142–153. [Google Scholar] [CrossRef]
- Llères, D.; James, J.; Swift, S.; Norman, D.G.; Lamond, A.I. Quantitative analysis of chromatin compaction in living cells using FLIM–FRET. J. Cell Biol. 2009, 187, 481–496. [Google Scholar] [CrossRef] [Green Version]
- Llères, D.; Bailly, A.P.; Perrin, A.; Norman, D.G.; Xirodimas, D.P.; Feil, R. Quantitative FLIM-FRET Microscopy to Monitor Nanoscale Chromatin Compaction in Vivo Reveals Structural Roles of Condensin Complexes. Cell Rep. 2017, 18, 1791–1803. [Google Scholar] [CrossRef] [Green Version]
- Llères, D.; Swift, S.; Lamond, A.I. Detecting Protein-Protein Interactions in Vivo with FRET using Multiphoton Fluorescence Lifetime Imaging Microscopy (FLIM). Curr. Protoc. Cytom. 2007, 42. [Google Scholar] [CrossRef] [PubMed]
- Kimura, H.; Cook, P.R. Kinetics of Core Histones in Living Human Cells. J. Cell Biol. 2001, 153, 1341–1354. [Google Scholar] [CrossRef] [PubMed]
- Lou, J.; Scipioni, L.; Wright, B.K.; Bartolec, T.K.; Zhang, J.; Masamsetti, V.P.; Gaus, K.; Gratton, E.; Cesare, A.J.; Hinde, E. Phasor histone FLIM-FRET microscopy quantifies spatiotemporal rearrangement of chromatin architecture during the DNA damage response. Proc. Natl. Acad. Sci. USA 2019, 116, 7323–7332. [Google Scholar] [CrossRef] [Green Version]
- Baarlink, C.; Plessner, M.; Sherrard, A.; Morita, K.; Misu, S.; Virant, D.; Kleinschnitz, E.-M.; Harniman, R.; Alibhai, D.; Baumeister, S.; et al. A transient pool of nuclear F-actin at mitotic exit controls chromatin organization. Nat. Cell Biol. 2017, 19, 1389–1399. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Sherrard, A.; Zhao, B.; Melak, M.; Trautwein, J.; Kleinschnitz, E.-M.; Tsopoulidis, N.; Fackler, O.T.; Schwan, C.; Grosse, R. GPCR-induced calcium transients trigger nuclear actin assembly for chromatin dynamics. Nat. Commun. 2019, 10, 5271. [Google Scholar] [CrossRef] [Green Version]
- Sobecki, M.; Mrouj, K.; Camasses, A.; Parisis, N.; Nicolas, E.; Llères, D.; Gerbe, F.; Prieto, S.; Krasinska, L.; David, A.; et al. The cell proliferation antigen Ki-67 organises heterochromatin. eLife 2016, 5, e13722. [Google Scholar] [CrossRef]
- Potapova, T.; Gorbsky, G.J. The Consequences of Chromosome Segregation Errors in Mitosis and Meiosis. Biology 2017, 6, 12. [Google Scholar] [CrossRef] [Green Version]
- Csankovszki, G.; Collette, K.; Spahl, K.; Carey, J.; Snyder, M.; Petty, E.; Patel, U.; Tabuchi, T.; Liu, H.; McLeod, I.; et al. Three Distinct Condensin Complexes Control C. elegans Chromosome Dynamics. Curr. Biol. 2009, 19, 9–19. [Google Scholar] [CrossRef] [Green Version]
- Ono, T.; Fang, Y.; Spector, D.L.; Hirano, T. Spatial and temporal regulation of Condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell 2004, 15, 3296–3308. [Google Scholar] [CrossRef]
- Albritton, S.E.; Ercan, S. Caenorhabditis elegans Dosage Compensation: Insights into Condensin-Mediated Gene Regulation. Trends Genet. TIG 2018, 34, 41–53. [Google Scholar] [CrossRef]
- Chan, R.C.; Severson, A.F.; Meyer, B.J. Condensin restructures chromosomes in preparation for meiotic divisions. J. Cell Biol. 2004, 167, 613–625. [Google Scholar] [CrossRef] [PubMed]
- Mets, D.G.; Meyer, B.J. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 2009, 139, 73–86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gonzalez-Serricchio, A.S.; Sternberg, P.W. Visualization of C. elegans transgenic arrays by GFP. BMC Genet. 2006, 7, 36. [Google Scholar] [CrossRef] [PubMed]
- Stear, J.H.; Roth, M.B. Characterization of HCP-6, a C. elegans protein required to prevent chromosome twisting and merotelic attachment. Genes Dev. 2002, 16, 1498–1508. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gumienny, T.L.; Lambie, E.; Hartwieg, E.; Horvitz, H.R.; Hengartner, M.O. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development 1999, 126, 1011–1022. [Google Scholar]
- Boulton, S.J.; Martin, J.S.; Polanowska, J.; Hill, D.E.; Gartner, A.; Vidal, M. BRCA1/BARD1 orthologs required for DNA repair in Caenorhabditis elegans. Curr. Biol. 2004, 14, 33–39. [Google Scholar] [CrossRef] [PubMed]
- O’Connell, K.F.; Leys, C.M.; White, J.G. A genetic screen for temperature-sensitive cell-division mutants of Caenorhabditis elegans. Genetics 1998, 149, 1303–1321. [Google Scholar] [PubMed]
- Marchetti, F.; Bishop, J.B.; Lowe, X.; Generoso, W.M.; Hozier, J.; Wyrobek, A.J. Etoposide induces heritable chromosomal aberrations and aneuploidy during male meiosis in the mouse. Proc. Natl. Acad. Sci. USA 2001, 98, 3952–3957. [Google Scholar] [CrossRef] [Green Version]
- Hughes, S.E.; Hawley, R.S. Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis. PLoS Genet. 2014, 10, e1004650. [Google Scholar] [CrossRef] [Green Version]
- Gómez, R.; Viera, A.; Berenguer, I.; Llano, E.; Pendás, A.M.; Barbero, J.L.; Kikuchi, A.; Suja, J.A. Cohesin removal precedes topoisomerase IIα-dependent decatenation at centromeres in male mammalian meiosis II. Chromosoma 2014, 123, 129–146. [Google Scholar] [CrossRef] [Green Version]
- Jaramillo-Lambert, A.; Fabritius, A.S.; Hansen, T.J.; Smith, H.E.; Golden, A. The Identification of a Novel Mutant Allele of topoisomerase II in Caenorhabditis elegans Reveals a Unique Role in Chromosome Segregation during Spermatogenesis. Genetics 2016, 204, 1407–1422. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haering, C.H.; Nasmyth, K. Building and breaking bridges between sister chromatids. BioEssays News Rev. Mol. Cell. Dev. Biol. 2003, 25, 1178–1191. [Google Scholar] [CrossRef] [PubMed]
- Rowley, M.J.; Nichols, M.H.; Lyu, X.; Ando-Kuri, M.; Rivera, I.S.M.; Hermetz, K.; Wang, P.; Ruan, Y.; Corces, V.G. Evolutionarily Conserved Principles Predict 3D Chromatin Organization. Mol. Cell 2017, 67, 837–852. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- van Steensel, B.; Furlong, E.E.M. The role of transcription in shaping the spatial organization of the genome. Nat. Rev. Mol. Cell Biol. 2019. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.A.-J.; Stempor, P.; Down, T.A.; Zeiser, E.; Feuer, S.K.; Ahringer, J. Extreme HOT regions are CpG-dense promoters in C. elegans and humans. Genome Res. 2014, 24, 1138–1146. [Google Scholar] [CrossRef] [Green Version]
- Simonet, T.; Dulermo, R.; Schott, S.; Palladino, F. Antagonistic functions of SET-2/SET1 and HPL/HP1 proteins in C. elegans development. Dev. Biol. 2007, 312, 367–383. [Google Scholar] [CrossRef] [Green Version]
- Christensen, J.; Agger, K.; Cloos, P.A.; Pasini, D.; Rose, S.; Sennels, L.; Rappsilber, J.; Hansen, K.H.; Salcini, A.E.; Helin, K. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007, 128, 1063–1076. [Google Scholar] [CrossRef] [Green Version]
- Alvares, S.M.; Mayberry, G.A.; Joyner, E.Y.; Lakowski, B.; Ahmed, S. H3K4 demethylase activities repress proliferative and postmitotic aging. Aging Cell 2014, 13, 245–253. [Google Scholar] [CrossRef]
- Samejima, K.; Samejima, I.; Vagnarelli, P.; Ogawa, H.; Vargiu, G.; Kelly, D.A.; de Lima-Alves, F.; Kerr, A.; Green, L.C.; Hudson, D.F.; et al. Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase IIα. J. Cell Biol. 2012, 199, 755–770. [Google Scholar] [CrossRef] [Green Version]
- Ganji, M.; Shaltiel, I.A.; Bisht, S.; Kim, E.; Kalichava, A.; Haering, C.H.; Dekker, C. Real-time imaging of DNA loop extrusion by condensin. Science 2018, 360, 102–105. [Google Scholar] [CrossRef] [Green Version]
- Gibcus, J.H.; Samejima, K.; Goloborodko, A.; Samejima, I.; Naumova, N.; Nuebler, J.; Kanemaki, M.T.; Xie, L.; Paulson, J.R.; Earnshaw, W.C.; et al. A pathway for mitotic chromosome formation. Science 2018, 359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wilkins, B.J.; Rall, N.A.; Ostwal, Y.; Kruitwagen, T.; Hiragami-Hamada, K.; Winkler, M.; Barral, Y.; Fischle, W.; Neumann, H. A Cascade of Histone Modifications Induces Chromatin Condensation in Mitosis. Science 2014, 343, 77–80. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vagnarelli, P.; Hudson, D.F.; Ribeiro, S.A.; Trinkle-Mulcahy, L.; Spence, J.M.; Lai, F.; Farr, C.J.; Lamond, A.I.; Earnshaw, W.C. Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 2006, 8, 1133–1142. [Google Scholar] [CrossRef] [PubMed]
- Georgatos, S.D.; Markaki, Y.; Christogianni, A.; Politou, A.S. Chromatin remodeling during mitosis: A structure-based code? Front. Biosci. Landmark Ed. 2009, 14, 2017–2027. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kruitwagen, T.; Denoth-Lippuner, A.; Wilkins, B.J.; Neumann, H.; Barral, Y. Axial contraction and short-range compaction of chromatin synergistically promote mitotic chromosome condensation. eLife 2015, 4, e1039. [Google Scholar] [CrossRef] [PubMed]
- Markaki, Y.; Christogianni, A.; Politou, A.S.; Georgatos, S.D. Phosphorylation of histone H3 at Thr3 is part of a combinatorial pattern that marks and configures mitotic chromatin. J. Cell Sci. 2009, 122, 2809–2819. [Google Scholar] [CrossRef] [Green Version]
- Zhiteneva, A.; Bonfiglio, J.J.; Makarov, A.; Colby, T.; Vagnarelli, P.; Schirmer, E.C.; Matic, I.; Earnshaw, W.C. Mitotic post-translational modifications of histones promote chromatin compaction in vitro. Open Biol. 2017, 7. [Google Scholar] [CrossRef] [Green Version]
- Ono, T.; Losada, A.; Hirano, M.; Myers, M.P.; Neuwald, A.F.; Hirano, T. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 2003, 115, 109–121. [Google Scholar] [CrossRef] [Green Version]
- Shi, Z.; Gao, H.; Bai, X.; Yu, H. Cryo-EM structure of the human cohesin-NIPBL-DNA complex. Science 2020, 368, 1454–1459. [Google Scholar] [CrossRef]
- Manalastas-Cantos, K.; Kschonsak, M.; Haering, C.H.; Svergun, D.I. Solution structure and flexibility of the condensin HEAT-repeat subunit Ycg1. J. Biol. Chem. 2019, 294, 13822–13829. [Google Scholar] [CrossRef]
- Kschonsak, M.; Merkel, F.; Bisht, S.; Metz, J.; Rybin, V.; Hassler, M.; Haering, C.H. Structural Basis for a Safety-Belt Mechanism That Anchors Condensin to Chromosomes. Cell 2017, 171, 588–600. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hong, Y.; Sonneville, R.; Agostinho, A.; Meier, B.; Wang, B.; Blow, J.J.; Gartner, A. The SMC-5/6 Complex and the HIM-6 (BLM) Helicase Synergistically Promote Meiotic Recombination Intermediate Processing and Chromosome Maturation during Caenorhabditis elegans Meiosis. PLoS Genet. 2016, 12, e1005872. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ladouceur, A.-M.; Ranjan, R.; Smith, L.; Fadero, T.; Heppert, J.; Goldstein, B.; Maddox, A.S.; Maddox, P.S. CENP-A and topoisomerase-II antagonistically affect chromosome length. J. Cell Biol. 2017, 216, 2645–2655. [Google Scholar] [CrossRef] [PubMed]
- Klein, F. Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J. Cell Biol. 1992, 117, 935–948. [Google Scholar] [CrossRef] [Green Version]
- Li, X.-M.; Yu, C.; Wang, Z.-W.; Zhang, Y.-L.; Liu, X.-M.; Zhou, D.; Sun, Q.-Y.; Fan, H.-Y. DNA Topoisomerase II Is Dispensable for Oocyte Meiotic Resumption but Is Essential for Meiotic Chromosome Condensation and Separation in Mice1. Biol. Reprod. 2013, 89. [Google Scholar] [CrossRef]
- Blat, Y.; Protacio, R.U.; Hunter, N.; Kleckner, N. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 2002, 111, 791–802. [Google Scholar] [CrossRef] [Green Version]
- McNicoll, F.; Stevense, M.; Jessberger, R. Cohesin in Gametogenesis. In Current Topics in Developmental Biology; Elsevier: Amsterdam, The Netherlands, 2013; Volume 102, pp. 1–34. ISBN 978-0-12-416024-8. [Google Scholar]
- Panizza, S.; Mendoza, M.A.; Berlinger, M.; Huang, L.; Nicolas, A.; Shirahige, K.; Klein, F. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 2011, 146, 372–383. [Google Scholar] [CrossRef] [Green Version]
- West, A.M.; Rosenberg, S.C.; Ur, S.N.; Lehmer, M.K.; Ye, Q.; Hagemann, G.; Caballero, I.; Usón, I.; MacQueen, A.J.; Herzog, F.; et al. A conserved filamentous assembly underlies the structure of the meiotic chromosome axis. eLife 2019, 8. [Google Scholar] [CrossRef]
- Prakash, K.; Fournier, D.; Redl, S.; Best, G.; Borsos, M.; Tiwari, V.K.; Tachibana-Konwalski, K.; Ketting, R.F.; Parekh, S.H.; Cremer, C.; et al. Superresolution imaging reveals structurally distinct periodic patterns of chromatin along pachytene chromosomes. Proc. Natl. Acad. Sci. USA 2015, 112, 14635–14640. [Google Scholar] [CrossRef] [Green Version]
- Patel, L.; Kang, R.; Rosenberg, S.C.; Qiu, Y.; Raviram, R.; Chee, S.; Hu, R.; Ren, B.; Cole, F.; Corbett, K.D. Dynamic reorganization of the genome shapes the recombination landscape in meiotic prophase. Nat. Struct. Mol. Biol. 2019, 26, 164–174. [Google Scholar] [CrossRef]
- Yuen, K.C.; Slaughter, B.D.; Gerton, J.L. Condensin II is anchored by TFIIIC and H3K4me3 in the mammalian genome and supports the expression of active dense gene clusters. Sci. Adv. 2017, 3, e1700191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Piskadlo, E.; Oliveira, R.A. Novel insights into mitotic chromosome condensation. F1000Research 2016, 5. [Google Scholar] [CrossRef] [PubMed]
- Brenner, S. The Genetics of Caenorhabditis elegans. Genetics 1974, 77, 71–94. [Google Scholar] [PubMed]
- Stringari, C.; Abdeladim, L.; Malkinson, G.; Mahou, P.; Solinas, X.; Lamarre, I.; Brizion, S.; Galey, J.-B.; Supatto, W.; Legouis, R.; et al. Multicolor two-photon imaging of endogenous fluorophores in living tissues by wavelength mixing. Sci. Rep. 2017, 7, 3792. [Google Scholar] [CrossRef]
- Förster, T. Experimental and theoretical investigation of the intermolecular transfer of electronic excitation energy. Z. Naturforsch. A 1949, 4, 321–327. [Google Scholar]
- Kadyk, L.C.; Kimble, J. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Dev. Camb. Engl. 1998, 125, 1803–1813. [Google Scholar]
- Heestand, B.; Simon, M.; Frenk, S.; Titov, D.; Ahmed, S. Transgenerational Sterility of Piwi Mutants Represents a Dynamic Form of Adult Reproductive Diapause. Cell Rep. 2018, 23, 156–171. [Google Scholar] [CrossRef] [Green Version]
- Papaluca, A.; Ramotar, D. A novel approach using C. elegans DNA damage-induced apoptosis to characterize the dynamics of uptake transporters for therapeutic drug discoveries. Sci. Rep. 2016, 6, 36026. [Google Scholar] [CrossRef]
- Schindelin, J.; Arganda-Carreras, I.; Frise, E.; Kaynig, V.; Longair, M.; Pietzsch, T.; Preibisch, S.; Rueden, C.; Saalfeld, S.; Schmid, B.; et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 2012, 9, 676–682. [Google Scholar] [CrossRef] [Green Version]
- Afgan, E.; Baker, D.; Batut, B.; van den Beek, M.; Bouvier, D.; Cech, M.; Chilton, J.; Clements, D.; Coraor, N.; Grüning, B.A.; et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 2018, 46, W537–W544. [Google Scholar] [CrossRef] [Green Version]
- Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Herbette, M.; Robert, V.; Bailly, A.; Gely, L.; Feil, R.; Llères, D.; Palladino, F. A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization. Cells 2020, 9, 2049. https://doi.org/10.3390/cells9092049
Herbette M, Robert V, Bailly A, Gely L, Feil R, Llères D, Palladino F. A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization. Cells. 2020; 9(9):2049. https://doi.org/10.3390/cells9092049
Chicago/Turabian StyleHerbette, Marion, Valérie Robert, Aymeric Bailly, Loïc Gely, Robert Feil, David Llères, and Francesca Palladino. 2020. "A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization" Cells 9, no. 9: 2049. https://doi.org/10.3390/cells9092049