The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance
Abstract
For most organisms, chromosome segregation during meiosis relies on deliberate induction of DNA double-strand breaks (DSBs) and repair of a subset of these DSBs as inter-homolog crossovers (COs). However, timing and levels of DSB formation must be tightly controlled to avoid jeopardizing genome integrity. Here we identify the DSB-2 protein, which is required for efficient DSB formation during C. elegans meiosis but is dispensable for later steps of meiotic recombination. DSB-2 localizes to chromatin during the time of DSB formation, and its disappearance coincides with a decline in RAD-51 foci marking early recombination intermediates and precedes appearance of COSA-1 foci marking CO-designated sites. These and other data suggest that DSB-2 and its paralog DSB-1 promote competence for DSB formation. Further, immunofluorescence analyses of wild-type gonads and various meiotic mutants reveal that association of DSB-2 with chromatin is coordinated with multiple distinct aspects of the meiotic program, including the phosphorylation state of nuclear envelope protein SUN-1 and dependence on RAD-50 to load the RAD-51 recombinase at DSB sites. Moreover, association of DSB-2 with chromatin is prolonged in mutants impaired for either DSB formation or formation of downstream CO intermediates. These and other data suggest that association of DSB-2 with chromatin ismore »
- Authors:
-
- Stanford University, CA (United States)
- University of California, Berkeley, CA (United States)
- University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Howard Hughes Medical Inst., Chevy Chase, MD (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); Leukemia and Lymphoma Society Fellowship; Helen Hay Whitney Foundation
- OSTI Identifier:
- 1627302
- Grant/Contract Number:
- AC02-05CH11231; T32 GM07790; R01 GM067268; P40 OD010440
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 9; Journal Issue: 8; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; chromatin; DNA repair; gonads; immunofluorescence; meiotic prophase; germ cells; nuclear staining; homologous
Citation Formats
Rosu, Simona, Zawadzki, Karl A., Stamper, Ericca L., Libuda, Diana E., Reese, Angela L., Dernburg, Abby F., and Villeneuve, Anne M. The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance. United States: N. p., 2013.
Web. doi:10.1371/journal.pgen.1003674.
Rosu, Simona, Zawadzki, Karl A., Stamper, Ericca L., Libuda, Diana E., Reese, Angela L., Dernburg, Abby F., & Villeneuve, Anne M. The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance. United States. https://doi.org/10.1371/journal.pgen.1003674
Rosu, Simona, Zawadzki, Karl A., Stamper, Ericca L., Libuda, Diana E., Reese, Angela L., Dernburg, Abby F., and Villeneuve, Anne M. Thu .
"The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance". United States. https://doi.org/10.1371/journal.pgen.1003674. https://www.osti.gov/servlets/purl/1627302.
@article{osti_1627302,
title = {The C. elegans DSB-2 Protein Reveals a Regulatory Network that Controls Competence for Meiotic DSB Formation and Promotes Crossover Assurance},
author = {Rosu, Simona and Zawadzki, Karl A. and Stamper, Ericca L. and Libuda, Diana E. and Reese, Angela L. and Dernburg, Abby F. and Villeneuve, Anne M.},
abstractNote = {For most organisms, chromosome segregation during meiosis relies on deliberate induction of DNA double-strand breaks (DSBs) and repair of a subset of these DSBs as inter-homolog crossovers (COs). However, timing and levels of DSB formation must be tightly controlled to avoid jeopardizing genome integrity. Here we identify the DSB-2 protein, which is required for efficient DSB formation during C. elegans meiosis but is dispensable for later steps of meiotic recombination. DSB-2 localizes to chromatin during the time of DSB formation, and its disappearance coincides with a decline in RAD-51 foci marking early recombination intermediates and precedes appearance of COSA-1 foci marking CO-designated sites. These and other data suggest that DSB-2 and its paralog DSB-1 promote competence for DSB formation. Further, immunofluorescence analyses of wild-type gonads and various meiotic mutants reveal that association of DSB-2 with chromatin is coordinated with multiple distinct aspects of the meiotic program, including the phosphorylation state of nuclear envelope protein SUN-1 and dependence on RAD-50 to load the RAD-51 recombinase at DSB sites. Moreover, association of DSB-2 with chromatin is prolonged in mutants impaired for either DSB formation or formation of downstream CO intermediates. These and other data suggest that association of DSB-2 with chromatin is an indicator of competence for DSB formation, and that cells respond to a deficit of CO-competent recombination intermediates by prolonging the DSB-competent state. In the context of this model, we propose that formation of sufficient CO-competent intermediates engages a negative feedback response that leads to cessation of DSB formation as part of a major coordinated transition in meiotic prophase progression. The proposed negative feedback regulation of DSB formation simultaneously (1) ensures that sufficient DSBs are made to guarantee CO formation and (2) prevents excessive DSB levels that could have deleterious effects.},
doi = {10.1371/journal.pgen.1003674},
journal = {PLoS Genetics},
number = 8,
volume = 9,
place = {United States},
year = {Thu Aug 08 00:00:00 EDT 2013},
month = {Thu Aug 08 00:00:00 EDT 2013}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
C. elegans HIM-17 Links Chromatin Modification and Competence for Initiation of Meiotic Recombination
journal, August 2004
- Reddy, Kirthi C.; Villeneuve, Anne M.
- Cell, Vol. 118, Issue 4
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans
journal, December 2005
- MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi
- Cell, Vol. 123, Issue 6
Functional genomic analysis of C. elegans chromosome I by systematic RNA interference
journal, November 2000
- Fraser, Andrew G.; Kamath, Ravi S.; Zipperlen, Peder
- Nature, Vol. 408, Issue 6810
xnd-1 regulates the global recombination landscape in Caenorhabditis elegans
journal, October 2010
- Wagner, Cynthia R.; Kuervers, Lynnette; Baillie, David L.
- Nature, Vol. 467, Issue 7317
HIM-8 Binds to the X Chromosome Pairing Center and Mediates Chromosome-Specific Meiotic Synapsis
journal, December 2005
- Phillips, Carolyn M.; Wong, Chihunt; Bhalla, Needhi
- Cell, Vol. 123, Issue 6
Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice
journal, June 2010
- Kumar, R.; Bourbon, H. -M.; de Massy, B.
- Genes & Development, Vol. 24, Issue 12
Meiotic Chromosome Homology Search Involves Modifications of the Nuclear Envelope Protein Matefin/SUN-1
journal, November 2009
- Penkner, Alexandra M.; Fridkin, Alexandra; Gloggnitzer, Jiradet
- Cell, Vol. 139, Issue 5
The Chk2 protein kinase
journal, August 2004
- Ahn, Jinwoo; Urist, Marshall; Prives, Carol
- DNA Repair, Vol. 3, Issue 8-9
A New Thermosensitive smc-3 Allele Reveals Involvement of Cohesin in Homologous Recombination in C. elegans
journal, September 2011
- Baudrimont, Antoine; Penkner, Alexandra; Woglar, Alexander
- PLoS ONE, Vol. 6, Issue 9
Mutations in Caenorhabditis elegans him-19 Show Meiotic Defects That Worsen with Age
journal, March 2010
- Tang, Lois; Machacek, Thomas; Mamnun, Yasmine M.
- Molecular Biology of the Cell, Vol. 21, Issue 6
Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2
journal, July 2001
- MacQueen, A. J.
- Genes & Development, Vol. 15, Issue 13
The Drosophila Zinc Finger Protein Trade Embargo Is Required for Double Strand Break Formation in Meiosis
journal, February 2011
- Lake, Cathleen M.; Nielsen, Rachel J.; Hawley, R. Scott
- PLoS Genetics, Vol. 7, Issue 2
Matefin/SUN-1 Phosphorylation Is Part of a Surveillance Mechanism to Coordinate Chromosome Synapsis and Recombination with Meiotic Progression and Chromosome Movement
journal, March 2013
- Woglar, Alexander; Daryabeigi, Anahita; Adamo, Adele
- PLoS Genetics, Vol. 9, Issue 3
Condensins Regulate Meiotic DNA Break Distribution, thus Crossover Frequency, by Controlling Chromosome Structure
journal, October 2009
- Mets, David G.; Meyer, Barbara J.
- Cell, Vol. 139, Issue 1
ATM controls meiotic double-strand-break formation
journal, October 2011
- Lange, Julian; Pan, Jing; Cole, Francesca
- Nature, Vol. 479, Issue 7372
HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans
journal, November 2005
- Couteau, F.
- Genes & Development, Vol. 19, Issue 22
Meiotic double-strand breaks occur once per pair of (sister) chromatids and, via Mec1/ATR and Tel1/ATM, once per quartet of chromatids
journal, November 2011
- Zhang, L.; Kim, K. P.; Kleckner, N. E.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 50
The Caenorhabditis elegansRAD51 homolog is transcribed into two alternative mRNAs potentially encoding proteins of different sizes
journal, November 1998
- Rinaldo, C.; Ederle, S.; Rocco, V.
- Molecular and General Genetics MGG, Vol. 260, Issue 2-3
Rapid single nucleotide polymorphism mapping in C. elegans
journal, September 2005
- Davis, M. Wayne; Hammarlund, Marc; Harrach, Tracey
- BMC Genomics, Vol. 6, Issue 1
HTP-3 Links DSB Formation with Homolog Pairing and Crossing Over during C. elegans Meiosis
journal, February 2008
- Goodyer, William; Kaitna, Susanne; Couteau, Florence
- Developmental Cell, Vol. 14, Issue 2
Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line
journal, August 2007
- Jaramillo-Lambert, Aimee; Ellefson, Marina; Villeneuve, Anne M.
- Developmental Biology, Vol. 308, Issue 1
Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans
journal, July 2003
- Alpi, Arno; Pasierbek, Pawel; Gartner, Anton
- Chromosoma, Vol. 112, Issue 1
EGL-10 Regulates G Protein Signaling in the C. elegans Nervous System and Shares a Conserved Domain with Many Mammalian Proteins
journal, January 1996
- Koelle, Michael R.; Horvitz, H. Robert
- Cell, Vol. 84, Issue 1
Domain-Specific Regulation of Recombination in Caenorhabditis elegans in Response to Temperature, Age and Sex
journal, September 2008
- Lim, Jaclyn G. Y.; Stine, Rachel R. W.; Yanowitz, Judith L.
- Genetics, Vol. 180, Issue 2
The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis
journal, June 2010
- Hayashi, Michiko; Mlynarczyk-Evans, Susanna; Villeneuve, Anne M.
- Genetics, Vol. 186, Issue 1
SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins
journal, January 2005
- Traven, Ana; Heierhorst, J�rg
- BioEssays, Vol. 27, Issue 4
Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map
journal, June 2001
- Wicks, Stephen R.; Yeh, Raymond T.; Gish, Warren R.
- Nature Genetics, Vol. 28, Issue 2
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans
journal, September 2002
- MacQueen, A. J.
- Genes & Development, Vol. 16, Issue 18
Mechanism and control of meiotic recombination initiation
book, January 2001
- Keeney, Scott
- Current Topics in Developmental Biology
Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in Caenorhabditis elegans
journal, November 2010
- Baudrimont, Antoine; Penkner, Alexandra; Woglar, Alexander
- PLoS Genetics, Vol. 6, Issue 11
HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis
journal, November 2005
- Martinez-Perez, E.
- Genes & Development, Vol. 19, Issue 22
Robust Crossover Assurance and Regulated Interhomolog Access Maintain Meiotic Crossover Number
journal, December 2011
- Rosu, S.; Libuda, D. E.; Villeneuve, A. M.
- Science, Vol. 334, Issue 6060
Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation
journal, September 1999
- Zetka, M. C.; Kawasaki, I.; Strome, S.
- Genes & Development, Vol. 13, Issue 17
The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation
journal, July 2009
- Severson, A. F.; Ling, L.; van Zuylen, V.
- Genes & Development, Vol. 23, Issue 15
Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis
journal, January 2012
- Wynne, David J.; Rog, Ofer; Carlton, Peter M.
- Journal of Cell Biology, Vol. 196, Issue 1
C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G2 DNA damage checkpoint
journal, March 2001
- Chin, G. M.
- Genes & Development, Vol. 15, Issue 5
Chromosome Choreography: The Meiotic Ballet
journal, August 2003
- Page, S. L.
- Science, Vol. 301, Issue 5634
Drosophila ATM and ATR have distinct activities in the regulation of meiotic DNA damage and repair
journal, October 2011
- Joyce, Eric F.; Pedersen, Michael; Tiong, Stanley
- Journal of Cell Biology, Vol. 195, Issue 3
A Role for Caenorhabditis elegans Chromatin-Associated Protein HIM-17 in the Proliferation vs . Meiotic Entry Decision
journal, January 2007
- Bessler, Jessica B.; Reddy, Kirthi C.; Hayashi, Michiko
- Genetics, Vol. 175, Issue 4
The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis
journal, June 2007
- Penkner, Alexandra; Tang, Lois; Novatchkova, Maria
- Developmental Cell, Vol. 12, Issue 6
Crossover Distribution and Frequency Are Regulated by him-5 in Caenorhabditis elegans
journal, April 2012
- Meneely, Philip M.; McGovern, Olivia L.; Heinis, Frazer I.
- Genetics, Vol. 190, Issue 4
Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis
journal, June 2009
- Wignall, Sarah M.; Villeneuve, Anne M.
- Nature Cell Biology, Vol. 11, Issue 7
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis
journal, November 2009
- Sato, Aya; Isaac, Berith; Phillips, Carolyn M.
- Cell, Vol. 139, Issue 5
C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression
journal, January 2005
- Hayashi, Michiko; Chin, Gregory M.; Villeneuve, Anne M.
- PLoS Genetics, Vol. preprint, Issue 2007
T-coffee: a novel method for fast and accurate multiple sequence alignment 1 1Edited by J. Thornton
journal, September 2000
- Notredame, Cédric; Higgins, Desmond G.; Heringa, Jaap
- Journal of Molecular Biology, Vol. 302, Issue 1
COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers
journal, March 2012
- Yokoo, Rayka; Zawadzki, Karl A.; Nabeshima, Kentaro
- Cell, Vol. 149, Issue 1
Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes
journal, November 2004
- Nabeshima, Kentaro; Villeneuve, Anne M.; Hillers, Kenneth J.
- Genetics, Vol. 168, Issue 3
Synapsis-Defective Mutants Reveal a Correlation Between Chromosome Conformation and the Mode of Double-Strand Break Repair During Caenorhabditis elegans Meiosis
journal, August 2007
- Smolikov, Sarit; Eizinger, Andreas; Hurlburt, Allison
- Genetics, Vol. 176, Issue 4
C. elegans Germ Cells Switch between Distinct Modes of Double-Strand Break Repair During Meiotic Prophase Progression
journal, November 2007
- Hayashi, Michiko; Chin, Gregory M.; Villeneuve, Anne M.
- PLoS Genetics, Vol. 3, Issue 11
Caenorhabditis elegans msh-5 Is Required for Both Normal and Radiation-Induced Meiotic Crossing Over but Not for Completion of Meiosis
journal, October 2000
- Kelly, Karen O.; Dernburg, Abby F.; Stanfield, Gillian M.
- Genetics, Vol. 156, Issue 2
A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans.
journal, March 1994
- Villeneuve, A. M.
- Genetics, Vol. 136, Issue 3
Chromosome Sites Play Dual Roles to Establish Homologous Synapsis during Meiosis in C. elegans
journal, December 2005
- MacQueen, Amy J.; Phillips, Carolyn M.; Bhalla, Needhi
- Cell, Vol. 123, Issue 6
When Size Does Not Matter: Pairing Sites during Meiosis
journal, December 2005
- McKim, Kim S.
- Cell, Vol. 123, Issue 6
Condensins Regulate Meiotic DNA Break Distribution, thus Crossover Frequency, by Controlling Chromosome Structure
journal, October 2009
- Mets, David G.; Meyer, Barbara J.
- Cell, Vol. 139, Issue 1
Cytoskeletal Forces Span the Nuclear Envelope to Coordinate Meiotic Chromosome Pairing and Synapsis
journal, November 2009
- Sato, Aya; Isaac, Berith; Phillips, Carolyn M.
- Cell, Vol. 139, Issue 5
COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers
journal, March 2012
- Yokoo, Rayka; Zawadzki, Karl A.; Nabeshima, Kentaro
- Cell, Vol. 149, Issue 1
The Nuclear Envelope Protein Matefin/SUN-1 Is Required for Homologous Pairing in C. elegans Meiosis
journal, June 2007
- Penkner, Alexandra; Tang, Lois; Novatchkova, Maria
- Developmental Cell, Vol. 12, Issue 6
HTP-3 Links DSB Formation with Homolog Pairing and Crossing Over during C. elegans Meiosis
journal, February 2008
- Goodyer, William; Kaitna, Susanne; Couteau, Florence
- Developmental Cell, Vol. 14, Issue 2
The Chk2 protein kinase
journal, August 2004
- Ahn, Jinwoo; Urist, Marshall; Prives, Carol
- DNA Repair, Vol. 3, Issue 8-9
Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line
journal, August 2007
- Jaramillo-Lambert, Aimee; Ellefson, Marina; Villeneuve, Anne M.
- Developmental Biology, Vol. 308, Issue 1
Meiotic Recombination in C. elegans Initiates by a Conserved Mechanism and Is Dispensable for Homologous Chromosome Synapsis
journal, August 1998
- Dernburg, Abby F.; McDonald, Kent; Moulder, Gary
- Cell, Vol. 94, Issue 3
Genome-wide RNAi screening in Caenorhabditis elegans
journal, August 2003
- Kamath, R.
- Methods, Vol. 30, Issue 4
Functional genomic analysis of C. elegans chromosome I by systematic RNA interference
journal, November 2000
- Fraser, Andrew G.; Kamath, Ravi S.; Zipperlen, Peder
- Nature, Vol. 408, Issue 6810
Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map
journal, June 2001
- Wicks, Stephen R.; Yeh, Raymond T.; Gish, Warren R.
- Nature Genetics, Vol. 28, Issue 2
xnd-1 regulates the global recombination landscape in Caenorhabditis elegans
journal, October 2010
- Wagner, Cynthia R.; Kuervers, Lynnette; Baillie, David L.
- Nature, Vol. 467, Issue 7317
ATM controls meiotic double-strand-break formation
journal, October 2011
- Lange, Julian; Pan, Jing; Cole, Francesca
- Nature, Vol. 479, Issue 7372
Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis
journal, June 2009
- Wignall, Sarah M.; Villeneuve, Anne M.
- Nature Cell Biology, Vol. 11, Issue 7
Dynein-dependent processive chromosome motions promote homologous pairing in C. elegans meiosis
journal, January 2012
- Wynne, David J.; Rog, Ofer; Carlton, Peter M.
- Journal of Cell Biology, Vol. 196, Issue 1
A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans.
journal, March 1994
- Villeneuve, A. M.
- Genetics, Vol. 136, Issue 3
Caenorhabditis elegans msh-5 Is Required for Both Normal and Radiation-Induced Meiotic Crossing Over but Not for Completion of Meiosis
journal, October 2000
- Kelly, Karen O.; Dernburg, Abby F.; Stanfield, Gillian M.
- Genetics, Vol. 156, Issue 2
Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans
journal, September 2002
- MacQueen, A. J.
- Genes & Development, Vol. 16, Issue 18
Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation
journal, September 1999
- Zetka, M. C.; Kawasaki, I.; Strome, S.
- Genes & Development, Vol. 13, Issue 17
HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis
journal, November 2005
- Martinez-Perez, E.
- Genes & Development, Vol. 19, Issue 22
HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans
journal, November 2005
- Couteau, F.
- Genes & Development, Vol. 19, Issue 22
The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation
journal, July 2009
- Severson, A. F.; Ling, L.; van Zuylen, V.
- Genes & Development, Vol. 23, Issue 15
Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice
journal, June 2010
- Kumar, R.; Bourbon, H. -M.; de Massy, B.
- Genes & Development, Vol. 24, Issue 12
C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G2 DNA damage checkpoint
journal, March 2001
- Chin, G. M.
- Genes & Development, Vol. 15, Issue 5
Robust Crossover Assurance and Regulated Interhomolog Access Maintain Meiotic Crossover Number
journal, December 2011
- Rosu, S.; Libuda, D. E.; Villeneuve, A. M.
- Science, Vol. 334, Issue 6060
Targeted Gene Knockout Reveals a Role in Meiotic Recombination for ZHP-3, a Zip3-Related Protein in Caenorhabditis elegans
journal, September 2004
- Jantsch, Verena; Pasierbek, Pawel; Mueller, Michael M.
- Molecular and Cellular Biology, Vol. 24, Issue 18
Rapid single nucleotide polymorphism mapping in C. elegans
journal, September 2005
- Davis, M. Wayne; Hammarlund, Marc; Harrach, Tracey
- BMC Genomics, Vol. 6, Issue 1
C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression
journal, January 2005
- Hayashi, Michiko; Chin, Gregory M.; Villeneuve, Anne M.
- PLoS Genetics, Vol. preprint, Issue 2007
Leptotene/Zygotene Chromosome Movement Via the SUN/KASH Protein Bridge in Caenorhabditis elegans
journal, November 2010
- Baudrimont, Antoine; Penkner, Alexandra; Woglar, Alexander
- PLoS Genetics, Vol. 6, Issue 11
A New Thermosensitive smc-3 Allele Reveals Involvement of Cohesin in Homologous Recombination in C. elegans
journal, September 2011
- Baudrimont, Antoine; Penkner, Alexandra; Woglar, Alexander
- PLoS ONE, Vol. 6, Issue 9
Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes
journal, November 2004
- Nabeshima, Kentaro; Villeneuve, Anne M.; Hillers, Kenneth J.
- Genetics, Vol. 168, Issue 3
A Role for Caenorhabditis elegans Chromatin-Associated Protein HIM-17 in the Proliferation vs . Meiotic Entry Decision
journal, January 2007
- Bessler, Jessica B.; Reddy, Kirthi C.; Hayashi, Michiko
- Genetics, Vol. 175, Issue 4
Domain-Specific Regulation of Recombination in Caenorhabditis elegans in Response to Temperature, Age and Sex
journal, September 2008
- Lim, Jaclyn G. Y.; Stine, Rachel R. W.; Yanowitz, Judith L.
- Genetics, Vol. 180, Issue 2
The Synaptonemal Complex Shapes the Crossover Landscape Through Cooperative Assembly, Crossover Promotion and Crossover Inhibition During Caenorhabditis elegans Meiosis
journal, June 2010
- Hayashi, Michiko; Mlynarczyk-Evans, Susanna; Villeneuve, Anne M.
- Genetics, Vol. 186, Issue 1
Crossover Distribution and Frequency Are Regulated by him-5 in Caenorhabditis elegans
journal, April 2012
- Meneely, Philip M.; McGovern, Olivia L.; Heinis, Frazer I.
- Genetics, Vol. 190, Issue 4
The phylogenetic relationships of Caenorhabditis and other rhabditids
journal, January 2005
- Kiontke, Karin
- WormBook
Works referencing / citing this record:
ATM and ATR Influence Meiotic Crossover Formation Through Antagonistic and Overlapping Functions in Caenorhabditis elegans
journal, April 2019
- Li, Wei; Yanowitz, Judith L.
- Genetics, Vol. 212, Issue 2
BRCA1-BARD1 associate with the synaptonemal complex and pro-crossover factors and influence RAD-51 dynamics during Caenorhabditis elegans meiosis
journal, November 2018
- Janisiw, Eva; Dello Stritto, Maria Rosaria; Jantsch, Verena
- PLOS Genetics, Vol. 14, Issue 11
DNA Damage Response and Spindle Assembly Checkpoint Function throughout the Cell Cycle to Ensure Genomic Integrity
journal, April 2015
- Lawrence, Katherine S.; Chau, Thinh; Engebrecht, JoAnne
- PLOS Genetics, Vol. 11, Issue 4
The conserved LEM-3/Ankle1 nuclease is involved in the combinatorial regulation of meiotic recombination repair and chromosome segregation in Caenorhabditis elegans
journal, June 2018
- Hong, Ye; Velkova, Maria; Silva, Nicola
- PLOS Genetics, Vol. 14, Issue 6
Meiotic Double-Strand Break Proteins Influence Repair Pathway Utilization
posted_content, July 2018
- Yanowitz, Judith L.; Macaisne, Nicolas; Kessler, Zebulin
- Genetics
Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4
journal, December 2018
- Kumar, Rajeev; Oliver, Cecilia; Brun, Christine
- Life Science Alliance, Vol. 1, Issue 6
Protein Phosphatase 4 Promotes Chromosome Pairing and Synapsis, and Contributes to Maintaining Crossover Competence with Increasing Age
journal, October 2014
- Sato-Carlton, Aya; Li, Xuan; Crawley, Oliver
- PLoS Genetics, Vol. 10, Issue 10
The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans
journal, November 2018
- Li, Qianyan; Saito, Takamune T.; Martinez-Garcia, Marina
- PLOS Genetics, Vol. 14, Issue 11
A compartmentalized signaling network mediates crossover control in meiosis
journal, March 2018
- Zhang, Liangyu; Köhler, Simone; Rillo-Bohn, Regina
- eLife, Vol. 7
Interdependent and separable functions of Caenorhabditis elegans MRN-C complex members couple formation and repair of meiotic DSBs
journal, April 2018
- Girard, Chloe; Roelens, Baptiste; Zawadzki, Karl A.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 19
ATM and ATR Influence Meiotic Crossover Formation Through Antagonistic and Overlapping Functions in C. elegans
posted_content, April 2019
- Li, Wei; Yanowitz, Judith
- Genetics
Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4
posted_content, July 2018
- Kumar, Rajeev; Oliver, Cecilia; Brun, Christine
- Life Science Alliance
Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes
journal, February 2019
- Subramanian, Vijayalakshmi V.; Zhu, Xuan; Markowitz, Tovah E.
- Nature Communications, Vol. 10, Issue 1
LINC complexes promote homologous recombination in part through inhibition of nonhomologous end joining
journal, December 2016
- Lawrence, Katherine S.; Tapley, Erin C.; Cruz, Victor E.
- The Journal of Cell Biology, Vol. 215, Issue 6
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation
posted_content, October 2017
- Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki
- The Journal of Cell Biology
Recombination suppression in heterozygotes for a pericentric inversion induces the interchromosomal effect on crossovers in Arabidopsis
journal, October 2019
- Termolino, Pasquale; Falque, Matthieu; Aiese Cigliano, Riccardo
- The Plant Journal, Vol. 100, Issue 6
The conserved LEM-3/Ankle1 nuclease is involved in the combinatorial regulation of meiotic recombination repair and chromosome segregation in Caenorhabditis elegans
posted_content, November 2017
- Hong, Ye; Velkova, Maria; Silva, Nicola
- PLOS Genetics
Persistent DNA-break potential near telomeres increases initiation of meiotic recombination on short chromosomes
posted_content, August 2018
- Subramanian, Vijayalakshmi V.; Zhu, Xuan; Markowitz, Tovah E.
- Nature Communications
The tumor suppressor BRCA1/BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans
posted_content, March 2018
- Li, Qianyan; Saito, Takamune T.; Deshong, Alison J.
- PLOS Genetics
Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis
journal, March 2017
- Pattabiraman, Divya; Roelens, Baptiste; Woglar, Alexander
- PLOS Genetics, Vol. 13, Issue 3
Meiotic Double-Strand Break Proteins Influence Repair Pathway Utilization
journal, September 2018
- Macaisne, Nicolas; Kessler, Zebulin; Yanowitz, Judith L.
- Genetics, Vol. 210, Issue 3
A chromatin-associated protein required for inducing and limiting meiotic DNA double-strand break formation
journal, October 2018
- Tian, Miao; Loidl, Josef
- Nucleic Acids Research
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation
journal, December 2017
- Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki
- Journal of Cell Biology, Vol. 217, Issue 2
Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation
posted_content, October 2017
- Sato-Carlton, Aya; Nakamura-Tabuchi, Chihiro; Chartrand, Stephane Kazuki
- The Journal of Cell Biology
Mouse REC114 is essential for meiotic DNA double-strand break formation and forms a complex with MEI4
posted_content, July 2018
- Kumar, Rajeev; Oliver, Cecilia; Brun, Christine
- Life Science Alliance
Evidence That Masking of Synapsis Imperfections Counterbalances Quality Control to Promote Efficient Meiosis
journal, December 2013
- Mlynarczyk-Evans, Susanna; Roelens, Baptiste; Villeneuve, Anne M.
- PLoS Genetics, Vol. 9, Issue 12
A Quality Control Mechanism Coordinates Meiotic Prophase Events to Promote Crossover Assurance
journal, April 2014
- Deshong, Alison J.; Ye, Alice L.; Lamelza, Piero
- PLoS Genetics, Vol. 10, Issue 4
Protein Phosphatase 4 Promotes Chromosome Pairing and Synapsis, and Contributes to Maintaining Crossover Competence with Increasing Age
journal, October 2014
- Sato-Carlton, Aya; Li, Xuan; Crawley, Oliver
- PLoS Genetics, Vol. 10, Issue 10
DNA Damage Response and Spindle Assembly Checkpoint Function throughout the Cell Cycle to Ensure Genomic Integrity
journal, April 2015
- Lawrence, Katherine S.; Chau, Thinh; Engebrecht, JoAnne
- PLOS Genetics, Vol. 11, Issue 4
Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis
journal, March 2017
- Pattabiraman, Divya; Roelens, Baptiste; Woglar, Alexander
- PLOS Genetics, Vol. 13, Issue 3
Vilya, a component of the recombination nodule, is required for meiotic double-strand break formation in Drosophila
journal, October 2015
- Lake, Cathleen M.; Nielsen, Rachel J.; Guo, Fengli
- eLife, Vol. 4
A compartmentalized signaling network mediates crossover control in meiosis
journal, March 2018
- Zhang, Liangyu; Köhler, Simone; Rillo-Bohn, Regina
- eLife, Vol. 7