Published 3 March 2003. doi:10.1083/jcb.200212080
© The Rockefeller University Press,
0021-9525/2003/3/657 $5.00
The Journal of Cell Biology, Volume 160, Number 5, 657-670
Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1ß and SMC3
Maureen Eijpe1,
Hildo Offenberg1,
Rolf Jessberger2,
Ekaterina Revenkova2 and
Christa Heyting1
1 Molecular Genetics Group, Wageningen University, 6703 BD Wageningen, Netherlands
2 Carl C. Icahn Institute for Gene Therapy and Molecular Medicine, Mt. Sinai School of Medicine, New York, NY 10029
Address correspondence to Christa Heyting, Molecular Genetics Group, Botanical Center, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, Netherlands. Tel.: 31-317-482150. Fax: 31-317-483146. E-mail: christa.heyting{at}wur.nl
In meiotic prophase, the sister chromatids of each chromosome develop a common axial element (AE) that is integrated into the synaptonemal complex (SC). We analyzed the incorporation of sister chromatid cohesion proteins (cohesins) and other AE components into AEs. Meiotic cohesin REC8 appeared shortly before premeiotic S phase in the nucleus and formed AE-like structures (REC8-AEs) from premeiotic S phase on. Subsequently, meiotic cohesin SMC1ß, cohesin SMC3, and AE proteins SCP2 and SCP3 formed dots along REC8-AEs, which extended and fused until they lined REC8-AEs along their length. In metaphase I, SMC1ß, SMC3, SCP2, and SCP3 disappeared from the chromosome arms and accumulated around the centromeres, where they stayed until anaphase II. In striking contrast, REC8 persisted along the chromosome arms until anaphase I and near the centromeres until anaphase II. We propose that REC8 provides a basis for AE formation and that the first steps in AE assembly do not require SMC1ß, SMC3, SCP2, and SCP3. Furthermore, SMC1ß, SMC3, SCP2, and SCP3 cannot provide arm cohesion during metaphase I. We propose that REC8 then provides cohesion. RAD51 and/or DMC1 coimmunoprecipitates with REC8, suggesting that REC8 may also provide a basis for assembly of recombination complexes.
Key Words: meiosis; axial element; rat; sister chromatid cohesion; synaptonemal complex

CiteULike
Complore
Connotea
Del.icio.us
Digg
Reddit
Technorati What's this?
This article has been cited by other articles:
-
Storlazzi, A., Tesse, S., Ruprich-Robert, G., Gargano, S., Poggeler, S., Kleckner, N., Zickler, D.
(2008). Coupling meiotic chromosome axis integrity to recombination. Genes Dev.
22: 796-809
[Abstract]
[Full Text]
-
Novak, I., Wang, H., Revenkova, E., Jessberger, R., Scherthan, H., Hoog, C.
(2008). Cohesin Smc1 determines meiotic chromatin axis loop organization. J. Cell Biol.
180: 83-90
[Abstract]
[Full Text]
-
Khetani, R. S., Bickel, S. E.
(2007). Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J. Cell Sci.
120: 3123-3137
[Abstract]
[Full Text]
-
Bolcun-Filas, E., Costa, Y., Speed, R., Taggart, M., Benavente, R., De Rooij, D. G, Cooke, H. J
(2007). SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol.
176: 741-747
[Abstract]
[Full Text]
-
Rockmill, B., Voelkel-Meiman, K., Roeder, G. S.
(2006). Centromere-Proximal Crossovers Are Associated With Precocious Separation of Sister Chromatids During Meiosis in Saccharomyces cerevisiae. Genetics
174: 1745-1754
[Abstract]
[Full Text]
-
Ding, D.-Q., Sakurai, N., Katou, Y., Itoh, T., Shirahige, K., Haraguchi, T., Hiraoka, Y.
(2006). Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J. Cell Biol.
174: 499-508
[Abstract]
[Full Text]
-
Novak, I., Lightfoot, D. A., Wang, H., Eriksson, A., Mahdy, E., Hoog, C.
(2006). Mouse Embryonic Stem Cells Form Follicle-Like Ovarian Structures but Do Not Progress Through Meiosis. Stem Cells
24: 1931-1936
[Abstract]
[Full Text]
-
de Boer, E., Stam, P., Dietrich, A. J. J., Pastink, A., Heyting, C.
(2006). Two levels of interference in mouse meiotic recombination. Proc. Natl. Acad. Sci. USA
103: 9607-9612
[Abstract]
[Full Text]
-
Roig, I., Garcia, R., Robles, P., Cortvrindt, R., Egozcue, J., Smitz, J., Garcia, M.
(2006). Human fetal ovarian culture permits meiotic progression and chromosome pairing process. Hum Reprod
21: 1359-1367
[Abstract]
[Full Text]
-
Liu, Z., Makaroff, C. A.
(2006). Arabidopsis Separase AESP Is Essential for Embryo Development and the Release of Cohesin during Meiosis. Plant Cell
18: 1213-1225
[Abstract]
[Full Text]
-
McCracken, S., Longman, D., Marcon, E., Moens, P., Downey, M., Nickerson, J. A., Jessberger, R., Wilde, A., Caceres, J. F., Emili, A., Blencowe, B. J.
(2005). Proteomic Analysis of SRm160-containing Complexes Reveals a Conserved Association with Cohesin. J. Biol. Chem.
280: 42227-42236
[Abstract]
[Full Text]
-
Revenkova, E, Jessberger, R
(2005). Keeping sister chromatids together: cohesins in meiosis. Reproduction
130: 783-790
[Abstract]
[Full Text]
-
Chelysheva, L., Diallo, S., Vezon, D., Gendrot, G., Vrielynck, N., Belcram, K., Rocques, N., Marquez-Lema, A., Bhatt, A. M., Horlow, C., Mercier, R., Mezard, C., Grelon, M.
(2005). AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J. Cell Sci.
118: 4621-4632
[Abstract]
[Full Text]
-
Trelles-Sticken, E., Adelfalk, C., Loidl, J., Scherthan, H.
(2005). Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol.
170: 213-223
[Abstract]
[Full Text]
-
Lam, W. S., Yang, X., Makaroff, C. A.
(2005). Characterization of Arabidopsis thaliana SMC1 and SMC3: evidence that AtSMC3 may function beyond chromosome cohesion. J. Cell Sci.
118: 3037-3048
[Abstract]
[Full Text]
-
Costa, Y., Speed, R., Ollinger, R., Alsheimer, M., Semple, C. A., Gautier, P., Maratou, K., Novak, I., Hoog, C., Benavente, R., Cooke, H. J.
(2005). Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci.
118: 2755-2762
[Abstract]
[Full Text]
-
Losada, A., Hirano, T.
(2005). Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev.
19: 1269-1287
[Abstract]
[Full Text]
-
de Vries, F. A.T., de Boer, E., van den Bosch, M., Baarends, W. M., Ooms, M., Yuan, L., Liu, J.-G., van Zeeland, A. A., Heyting, C., Pastink, A.
(2005). Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev.
19: 1376-1389
[Abstract]
[Full Text]
-
Page, J., Berrios, S., Parra, M. T., Viera, A., Suja, J. A., Prieto, I., Barbero, J. L., Rufas, J. S., Fernandez-Donoso, R.
(2005). The Program of Sex Chromosome Pairing in Meiosis Is Highly Conserved Across Marsupial Species: Implications for Sex Chromosome Evolution. Genetics
170: 793-799
[Abstract]
[Full Text]
-
Li, W., Yang, X., Lin, Z., Timofejeva, L., Xiao, R., Makaroff, C. A., Ma, H.
(2005). The AtRAD51C Gene Is Required for Normal Meiotic Chromosome Synapsis and Double-Stranded Break Repair in Arabidopsis. Plant Physiol.
138: 965-976
[Abstract]
[Full Text]
-
Kouznetsova, A., Novak, I., Jessberger, R., Hoog, C.
(2005). SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J. Cell Sci.
118: 2271-2278
[Abstract]
[Full Text]
-
Roig, I, Robles, P, Garcia, R, Martinez-Flores, I, Cabero, L., Egozcue, J, Liebe, B, Scherthan, H, Garcia, M
(2005). Chromosome 18 pairing behavior in human trisomic oocytes. Presence of an extra chromosome extends bouquet stage. Reproduction
129: 565-575
[Abstract]
[Full Text]
-
Anderson, L. K., Royer, S. M., Page, S. L., McKim, K. S., Lai, A., Lilly, M. A., Hawley, R. S.
(2005). Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc. Natl. Acad. Sci. USA
102: 4482-4487
[Abstract]
[Full Text]
-
Firooznia, A., Revenkova, E., Jessberger, R.
(2005). From the XXVII North American Testis Workshop: The Function of SMC and Other Cohesin Proteins in Meiosis. J Androl
26: 1-10
[Full Text]
-
Watanabe, Y.
(2004). Modifying sister chromatid cohesion for meiosis. J. Cell Sci.
117: 4017-4023
[Abstract]
[Full Text]
-
Parra, M. T., Viera, A., Gomez, R., Page, J., Benavente, R., Santos, J. L., Rufas, J. S., Suja, J. A.
(2004). Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J. Cell Sci.
117: 1221-1234
[Abstract]
[Full Text]
-
Liebe, B., Alsheimer, M., Hoog, C., Benavente, R., Scherthan, H.
(2004). Telomere Attachment, Meiotic Chromosome Condensation, Pairing, and Bouquet Stage Duration Are Modified in Spermatocytes Lacking Axial Elements. Mol. Biol. Cell
15: 827-837
[Abstract]
[Full Text]
-
Kwon, Y. T., Xia, Z., An, J. Y., Tasaki, T., Davydov, I. V., Seo, J. W., Sheng, J., Xie, Y., Varshavsky, A.
(2003). Female Lethality and Apoptosis of Spermatocytes in Mice Lacking the UBR2 Ubiquitin Ligase of the N-End Rule Pathway. Mol. Cell. Biol.
23: 8255-8271
[Abstract]
[Full Text]
-
Voet, T., Liebe, B., Labaere, C., Marynen, P., Scherthan, H.
(2003). Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis. J. Cell Biol.
162: 795-808
[Abstract]
[Full Text]
-
Page, S. L., Hawley, R. S.
(2003). Chromosome Choreography: The Meiotic Ballet. Science
301: 785-789
[Abstract]
[Full Text]