|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | |||||
Research Article |
1 Department of Biology, York University, Toronto, ON, M3J 1P3, Canada
2 Imperial Cancer Research Fund, South Hall Laboratories, South Mimms,
Hertfordshire, England EN6 3LD
3 Dept of Molecular Genetics, Albert Einstein College of Medicine, New York
10461 USA
* Author for correspondence (e-mail: moens{at}yorku.ca )
Accepted 11 December 2001
During mouse meiosis, the early prophase RAD51/DMC1 recombination protein sites, which are associated with the chromosome cores and which serve as markers for ongoing DNA-DNA interactions, are in ten-fold excess of the eventual reciprocal recombinant events. Most, if not all, of these early interactions are eliminated as prophase progresses. The manner in which these sites are eliminated is the focus of this investigation. We report that these sites acquire replication protein A, RPA and the Escherichia coli MUTS homologue, MSH4p, and somewhat later the Bloom helicase, BLM, while simultaneously losing the RAD51/DMC1 component. Eventually the RPA component is also lost and BLM sites remain. At that time, the MUTL homologue, MLH1p, which is essential for reciprocal recombination in the mouse, appears in numbers and locations that correspond to the distribution of reciprocal recombination events. However, the MLH1 foci do not appear to coincide with the remaining BLM sites. The MLH1p is specifically localized to electron-microscope-defined recombination nodules. We consider the possibility that the homology-search RAD51/DMC1 complexes are involved in homologous chromosome synapsis but that most of these early DNA-DNA interactions are later resolved by the anti-recombination RPA/MSH4/BLM-topoisomerase complex, thereby preventing the formation of superfluous reciprocal recombinant events.
Key words: Meiosis, Recombination proteins, Immunocytology, Synaptonemal complexes, BLM, RPA, MLH1, Mouse, Recombination nodules
Related articles in JCS:
This article has been cited by other articles:
![]() |
T. Sasaki, E. Marcon, T. McQuire, Y. Arai, P. B. Moens, and H. Okada Bat3 deficiency accelerates the degradation of Hsp70-2/HspA2 during spermatogenesis J. Cell Biol., August 11, 2008; 182(3): 449 - 458. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Hamer, H. Wang, E. Bolcun-Filas, H. J. Cooke, R. Benavente, and C. Hoog Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex J. Cell Sci., August 1, 2008; 121(15): 2445 - 2451. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. T. Nishant, A. J. Plys, and E. Alani A Mutation in the Putative MLH3 Endonuclease Domain Confers a Defect in Both Mismatch Repair and Meiosis in Saccharomyces cerevisiae Genetics, June 1, 2008; 179(2): 747 - 755. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Yang, K. Gell, G. W. van der Heijden, S. Eckardt, N. A. Leu, D. C. Page, R. Benavente, C. Her, C. Hoog, K. J. McLaughlin, et al. Meiotic failure in male mice lacking an X-linked factor Genes & Dev., March 1, 2008; 22(5): 682 - 691. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Yang, S. Eckardt, N. A. Leu, K. J. McLaughlin, and P. J. Wang Mouse TEX15 is essential for DNA double-strand break repair and chromosomal synapsis during male meiosis J. Cell Biol., February 25, 2008; 180(4): 673 - 679. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Snowden, K.-S. Shim, C. Schmutte, S. Acharya, and R. Fishel hMSH4-hMSH5 Adenosine Nucleotide Processing and Interactions with Homologous Recombination Machinery J. Biol. Chem., January 4, 2008; 283(1): 145 - 154. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Oliver-Bonet, M. Campillo, P. J. Turek, E. Ko, and R.H. Martin Analysis of replication protein A (RPA) in human spermatogenesis Mol. Hum. Reprod., December 1, 2007; 13(12): 837 - 844. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Sanchez-Moran, J.-L. Santos, G. H. Jones, and F. C. H. Franklin ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis Genes & Dev., September 1, 2007; 21(17): 2220 - 2233. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Falque, R. Mercier, C. Mezard, D. de Vienne, and O. C. Martin Patterns of Recombination and MLH1 Foci Density Along Mouse Chromosomes: Modeling Effects of Interference and Obligate Chiasma Genetics, July 1, 2007; 176(3): 1453 - 1467. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Chicheportiche, J. Bernardino-Sgherri, B. de Massy, and B. Dutrillaux Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse J. Cell Sci., May 15, 2007; 120(10): 1733 - 1742. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Terasawa, H. Ogawa, Y. Tsukamoto, M. Shinohara, K. Shirahige, N. Kleckner, and T. Ogawa Meiotic recombination-related DNA synthesis and its implications for cross-over and non-cross-over recombinant formation PNAS, April 3, 2007; 104(14): 5965 - 5970. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. B. Moens, E. Marcon, J. S. Shore, N. Kochakpour, and B. Spyropoulos Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes J. Cell Sci., March 15, 2007; 120(6): 1017 - 1027. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. G.P. Lhuissier, H. H. Offenberg, P. E. Wittich, N. O.E. Vischer, and C. Heyting The Mismatch Repair Protein MLH1 Marks a Subset of Strongly Interfering Crossovers in Tomato PLANT CELL, March 1, 2007; 19(3): 862 - 876. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. de Boer, P. Stam, A. J. J. Dietrich, A. Pastink, and C. Heyting Two levels of interference in mouse meiotic recombination PNAS, June 20, 2006; 103(25): 9607 - 9612. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. E. Cohen, S. E. Pollack, and J. W. Pollard Genetic Analysis of Chromosome Pairing, Recombination, and Cell Cycle Control during First Meiotic Prophase in Mammals Endocr. Rev., June 1, 2006; 27(4): 398 - 426. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Wang and C. Hoog Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes J. Cell Biol., May 22, 2006; 173(4): 485 - 495. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Ma, K.A. Ferguson, S. Arsovska, P. Moens, and V. Chow Reduced recombination associated with the production of aneuploid sperm in an infertile man: a case report Hum. Reprod., April 1, 2006; 21(4): 980 - 985. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. P. Greenbaum, W. Yan, M.-H. Wu, Y.-N. Lin, J. E. Agno, M. Sharma, R. E. Braun, A. Rajkovic, and M. M. Matzuk TEX14 is essential for intercellular bridges and fertility in male mice PNAS, March 28, 2006; 103(13): 4982 - 4987. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A Morelli and P. E Cohen Not all germ cells are created equal: Aspects of sexual dimorphism in mammalian meiosis Reproduction, December 1, 2005; 130(6): 761 - 781. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. K. Kolas, A. Svetlanov, M. L. Lenzi, F. P. Macaluso, S. M. Lipkin, R. M. Liskay, J. Greally, W. Edelmann, and P. E. Cohen Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I J. Cell Biol., November 7, 2005; 171(3): 447 - 458. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Sun, M. Oliver-Bonet, T. Liehr, H. Starke, K. Trpkov, E. Ko, A. Rademaker, and R. H. Martin Discontinuities and unsynapsed regions in meiotic chromosomes have a cis effect on meiotic recombination patterns in normal human males Hum. Mol. Genet., October 15, 2005; 14(20): 3013 - 3018. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Calvente, A. Viera, J. Page, M. T. Parra, R. Gomez, J. A. Suja, J. S. Rufas, and J. L. Santos DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis J. Cell Sci., July 1, 2005; 118(13): 2957 - 2963. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Oliver-Bonet, P.J. Turek, F. Sun, E. Ko, and R.H. Martin Temporal progression of recombination in human males Mol. Hum. Reprod., July 1, 2005; 11(7): 517 - 522. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. A.T. de Vries, E. de Boer, M. van den Bosch, W. M. Baarends, M. Ooms, L. Yuan, J.-G. Liu, A. A. van Zeeland, C. Heyting, and A. Pastink Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation Genes & Dev., June 1, 2005; 19(11): 1376 - 1389. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. Li, X. Yang, Z. Lin, L. Timofejeva, R. Xiao, C. A. Makaroff, and H. Ma The AtRAD51C Gene Is Required for Normal Meiotic Chromosome Synapsis and Double-Stranded Break Repair in Arabidopsis Plant Physiology, June 1, 2005; 138(2): 965 - 976. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. L. Argueso, J. Wanat, Z. Gemici, and E. Alani Competing Crossover Pathways Act During Meiosis in Saccharomyces cerevisiae Genetics, December 1, 2004; 168(4): 1805 - 1816. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Neyton, F. Lespinasse, P. B. Moens, R. Paul, P. Gaudray, V. Paquis-Flucklinger, and S. Santucci-Darmanin Association between MSH4 (MutS homologue 4) and the DNA strand-exchange RAD51 and DMC1 proteins during mammalian meiosis Mol. Hum. Reprod., December 1, 2004; 10(12): 917 - 924. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Nabeshima, A. M. Villeneuve, and K. J. Hillers Chromosome-Wide Regulation of Meiotic Crossover Formation in Caenorhabditis elegans Requires Properly Assembled Chromosome Axes Genetics, November 1, 2004; 168(3): 1275 - 1292. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Sanchez-Moran, G. H. Jones, F. C. H. Franklin, and J. L. Santos A Puromycin-Sensitive Aminopeptidase Is Essential for Meiosis in Arabidopsis thaliana PLANT CELL, November 1, 2004; 16(11): 2895 - 2909. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Higgins, S. J. Armstrong, F. C. H. Franklin, and G. H. Jones The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis Genes & Dev., October 15, 2004; 18(20): 2557 - 2570. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. W. Stahl, H. M. Foss, L. S. Young, R. H. Borts, M. F. F. Abdullah, and G. P. Copenhaver Does Crossover Interference Count in Saccharomyces cerevisiae? Genetics, September 1, 2004; 168(1): 35 - 48. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Habu, N. Wakabayashi, K. Yoshida, K. Yomogida, Y. Nishimune, and T. Morita p53 protein interacts specifically with the meiosis-specific mammalian RecA-like protein DMC1 in meiosis Carcinogenesis, June 1, 2004; 25(6): 889 - 893. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Liu, S. Franco, B. Spyropoulos, P. B. Moens, M. A. Blasco, and D. L. Keefe Irregular telomeres impair meiotic synapsis and recombination in mice PNAS, April 27, 2004; 101(17): 6496 - 6501. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. K. Anderson, N. Salameh, H. W. Bass, L. C. Harper, W. Z. Cande, G. Weber, and S. M. Stack Integrating Genetic Linkage Maps With Pachytene Chromosome Structure in Maize Genetics, April 1, 2004; 166(4): 1923 - 1933. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Perera, L. Perez-Hidalgo, P. B. Moens, K. Reini, N. Lakin, J. E. Syvaoja, P. A. San-Segundo, and R. Freire TopBP1 and ATR Colocalization at Meiotic Chromosomes: Role of TopBP1/Cut5 in the Meiotic Recombination Checkpoint Mol. Biol. Cell, April 1, 2004; 15(4): 1568 - 1579. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Qin, L. L. Richardson, M. Jasin, M. A. Handel, and N. Arnheim Mouse Strains with an Active H2-Ea Meiotic Recombination Hot Spot Exhibit Increased Levels of H2-Ea-Specific DNA Breaks in Testicular Germ Cells Mol. Cell. Biol., February 15, 2004; 24(4): 1655 - 1666. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. P. Pawlowski, I. N. Golubovskaya, L. Timofejeva, R. B. Meeley, W. F. Sheridan, and W. Z. Cande Coordination of Meiotic Recombination, Pairing, and Synapsis by PHS1 Science, January 2, 2004; 303(5654): 89 - 92. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Barchi and M. Jasin Seeking new meiotic genes PNAS, December 23, 2003; 100(26): 15287 - 15289. [Full Text] [PDF] |
||||
![]() |
E. Marcon and P. Moens MLH1p and MLH3p Localize to Precociously Induced Chiasmata of Okadaic-Acid-Treated Mouse Spermatocytes Genetics, December 1, 2003; 165(4): 2283 - 2287. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Storlazzi, S. Tesse, S. Gargano, F. James, N. Kleckner, and D. Zickler Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division Genes & Dev., November 1, 2003; 17(21): 2675 - 2687. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. K. Anderson, G. G. Doyle, B. Brigham, J. Carter, K. D. Hooker, A. Lai, M. Rice, and S. M. Stack High-Resolution Crossover Maps for Each Bivalent of Zea mays Using Recombination Nodules Genetics, October 1, 2003; 165(2): 849 - 865. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. C.Y. Wong, N. Alon, C. Mckerlie, J. R. Huang, M. S. Meyn, and M. Buchwald Targeted disruption of exons 1 to 6 of the Fanconi Anemia group A gene leads to growth retardation, strain-specific microphthalmia, meiotic defects and primordial germ cell hypoplasia Hum. Mol. Genet., August 15, 2003; 12(16): 2063 - 2076. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. L. Page and R. S. Hawley Chromosome Choreography: The Meiotic Ballet Science, August 8, 2003; 301(5634): 785 - 789. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. P. Pawlowski, I. N. Golubovskaya, and W. Z. Cande Altered Nuclear Distribution of Recombination Protein RAD51 in Maize Mutants Suggests the Involvement of RAD51 in Meiotic Homology Recognition PLANT CELL, August 1, 2003; 15(8): 1807 - 1816. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Crackower, N. K. Kolas, J. Noguchi, R. Sarao, K. Kikuchi, H. Kaneko, E. Kobayashi, Y. Kawai, I. Kozieradzki, R. Landers, et al. Essential Role of Fkbp6 in Male Fertility and Homologous Chromosome Pairing in Meiosis Science, May 23, 2003; 300(5623): 1291 - 1295. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Xu, O. Aprelikova, P. Moens, C.-X. Deng, and P. A. Furth Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice Development, May 1, 2003; 130(9): 2001 - 2012. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Y. Kwan, P. B. Moens, and J. C. Wang Infertility and aneuploidy in mice lacking a type IA DNA topoisomerase IIIbeta PNAS, March 4, 2003; 100(5): 2526 - 2531. [Abstract] [Full Text] [PDF] |
||||
![]() |
W. M. Baarends, E. Wassenaar, J. W. Hoogerbrugge, G. van Cappellen, H. P. Roest, J. Vreeburg, M. Ooms, J. H. J. Hoeijmakers, and J. A. Grootegoed Loss of HR6B Ubiquitin-Conjugating Activity Results in Damaged Synaptonemal Complex Structure and Increased Crossing-Over Frequency during the Male Meiotic Prophase Mol. Cell. Biol., February 15, 2003; 23(4): 1151 - 1162. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Stark and M. Jasin Extensive Loss of Heterozygosity Is Suppressed during Homologous Repair of Chromosomal Breaks Mol. Cell. Biol., January 15, 2003; 23(2): 733 - 743. [Abstract] [Full Text] [PDF] |
||||