This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pelttari, J.
Right arrow Articles by Höög, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pelttari, J.
Right arrow Articles by Höög, C.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, August 2001, p. 5667-5677, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5667-5677.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

A Meiotic Chromosomal Core Consisting of Cohesin Complex Proteins Recruits DNA Recombination Proteins and Promotes Synapsis in the Absence of an Axial Element in Mammalian Meiotic Cells

Jeanette Pelttari,1 Mary-Rose Hoja,1 Li Yuan,1 Jian-Guo Liu,1 Eva Brundell,1 Peter Moens,2 Sabine Santucci-Darmanin,3 Rolf Jessberger,4 Jose Luis Barbero,5 Christa Heyting,6 and Christer Höög1,*

Department of Cell and Molecular Biology and Center for Genomics Research, Karolinska Institutet, S-171 77 Stockholm, Sweden1; Department of Biology, York University, Toronto, Ontario M3J 1P3, Canada2; Laboratorie de Neurobiologie Cellulaire, UMR CNRS/UNSA 6549, Faculté de Médecine, 06107 Nice cedex 2, France3; Institute for Gene Therapy and Molecular Medicine, Mount Sinai School of Medicine, New York, New York 10029-65744; Department of Immunology and Oncology, Centro Nacional de Biotecnologia, UAM Campus Cantoblanco, Madrid E-28049, Spain5; and Laboratory of Genetics, Wageningen University, NL-6703HA Wageningen, The Netherlands6

Received 8 March 2001/Returned for modification 27 April 2001/Accepted 7 May 2001

The behavior of meiotic chromosomes differs in several respects from that of their mitotic counterparts, resulting in the generation of genetically distinct haploid cells. This has been attributed in part to a meiosis-specific chromatin-associated protein structure, the synaptonemal complex. This complex consist of two parallel axial elements, each one associated with a pair of sister chromatids, and a transverse filament located between the synapsed homologous chromosomes. Recently, a different protein structure, the cohesin complex, was shown to be associated with meiotic chromosomes and to be required for chromosome segregation. To explore the functions of the two different protein structures, the synaptonemal complex and the cohesin complex, in mammalian male meiotic cells, we have analyzed how absence of the axial element affects early meiotic chromosome behavior. We find that the synaptonemal complex protein 3 (SCP3) is a main determinant of axial-element assembly and is required for attachment of this structure to meiotic chromosomes, whereas SCP2 helps shape the in vivo structure of the axial element. We also show that formation of a cohesin-containing chromosomal core in meiotic nuclei does not require SCP3 or SCP2. Our results also suggest that the cohesin core recruits recombination proteins and promotes synapsis between homologous chromosomes in the absence of an axial element. A model for early meiotic chromosome pairing and synapsis is proposed.


* Corresponding author. Mailing address: Department of Cell and Molecular Biology, Medical Nobel Institute, Karolinska Institutet, S-171 77 Stockholm, Sweden. Phone: 46-8-7287365. Fax: 48-8-313529. E-mail: christer.hoog{at}cmb.ki.se.


Molecular and Cellular Biology, August 2001, p. 5667-5677, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5667-5677.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Brieno-Enriquez, M.A., Robles, P., Garcia-Cruz, R., Roig, I., Cabero, L., Martinez, F., Garcia Caldes, M. (2009). A new culture technique that allows in vitro meiotic prophase development of fetal human oocytes. Hum Reprod 0: dep351v1-dep351 [Abstract] [Full Text]  
  • Kouznetsova, A., Wang, H., Bellani, M., Camerini-Otero, R. D., Jessberger, R., Hoog, C. (2009). BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asynapsed chromosomes. J. Cell Sci. 122: 2446-2452 [Abstract] [Full Text]  
  • Hamer, G., Wang, H., Bolcun-Filas, E., Cooke, H. J., Benavente, R., Hoog, C. (2008). Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J. Cell Sci. 121: 2445-2451 [Abstract] [Full Text]  
  • Novak, I., Wang, H., Revenkova, E., Jessberger, R., Scherthan, H., Hoog, C. (2008). Cohesin Smc1 determines meiotic chromatin axis loop organization. JCB 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. JCB 176: 741-747 [Abstract] [Full Text]  
  • Danner, S., Kajahn, J., Geismann, C., Klink, E., Kruse, C. (2007). Derivation of oocyte-like cells from a clonal pancreatic stem cell line. Mol Hum Reprod 13: 11-20 [Abstract] [Full Text]  
  • Hamer, G., Gell, K., Kouznetsova, A., Novak, I., Benavente, R., Hoog, C. (2006). Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J. Cell Sci. 119: 4025-4032 [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. JCB 174: 499-508 [Abstract] [Full Text]  
  • Yang, F., Fuente, R. D. L., Leu, N. A., Baumann, C., McLaughlin, K. J., Wang, P. J. (2006). Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. JCB 173: 497-507 [Abstract] [Full Text]  
  • Nonomura, K.-I., Nakano, M., Eiguchi, M., Suzuki, T., Kurata, N. (2006). PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J. Cell Sci. 119: 217-225 [Abstract] [Full Text]  
  • Revenkova, E, Jessberger, R (2005). Keeping sister chromatids together: cohesins in meiosis. Reproduction 130: 783-790 [Abstract] [Full Text]  
  • Calvente, A., Viera, A., Page, J., Parra, M. T., Gomez, R., Suja, J. A., Rufas, J. S., Santos, J. L. (2005). DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis. J. Cell Sci. 118: 2957-2963 [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]  
  • 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]  
  • 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]  
  • Ollinger, R., Alsheimer, M., Benavente, R. (2005). Mammalian Protein SCP1 Forms Synaptonemal Complex-like Structures in the Absence of Meiotic Chromosomes. Mol. Biol. Cell 16: 212-217 [Abstract] [Full Text]  
  • Watanabe, Y. (2004). Modifying sister chromatid cohesion for meiosis. J. Cell Sci. 117: 4017-4023 [Abstract] [Full Text]  
  • Liu, L., Franco, S., Spyropoulos, B., Moens, P. B., Blasco, M. A., Keefe, D. L. (2004). Irregular telomeres impair meiotic synapsis and recombination in mice. Proc. Natl. Acad. Sci. USA 101: 6496-6501 [Abstract] [Full Text]  
  • Perera, D., Perez-Hidalgo, L., Moens, P. B., Reini, K., Lakin, N., Syvaoja, J. E., San-Segundo, P. A., Freire, R. (2004). TopBP1 and ATR Colocalization at Meiotic Chromosomes: Role of TopBP1/Cut5 in the Meiotic Recombination Checkpoint. Mol. Biol. Cell 15: 1568-1579 [Abstract] [Full Text]  
  • Webber, H. A., Howard, L., Bickel, S. E. (2004). The cohesion protein ORD is required for homologue bias during meiotic recombination. JCB 164: 819-829 [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]  
  • Anderson, L. K., Doyle, G. G., Brigham, B., Carter, J., Hooker, K. D., Lai, A., Rice, M., Stack, S. M. (2003). High-Resolution Crossover Maps for Each Bivalent of Zea mays Using Recombination Nodules. Genetics 165: 849-865 [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. JCB 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]  
  • Mercier, R., Armstrong, Susan. J., Horlow, C., Jackson, N. P., Makaroff, C. A., Vezon, D., Pelletier, G., Jones, G. H., Franklin, F. C. H. (2003). The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130: 3309-3318 [Abstract] [Full Text]  
  • Lee, J., Iwai, T., Yokota, T., Yamashita, M. (2003). Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis. J. Cell Sci. 116: 2781-2790 [Abstract] [Full Text]  
  • Eijpe, M., Offenberg, H., Jessberger, R., Revenkova, E., Heyting, C. (2003). Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1{beta} and SMC3. JCB 160: 657-670 [Abstract] [Full Text]  
  • Santucci-Darmanin, S., Neyton, S., Lespinasse, F., Saunieres, A., Gaudray, P., Paquis-Flucklinger, V. (2002). The DNA mismatch-repair MLH3 protein interacts with MSH4 in meiotic cells, supporting a role for this MutL homolog in mammalian meiotic recombination. Hum Mol Genet 11: 1697-1706 [Abstract] [Full Text]  
  • Yuan, L., Liu, J.-G., Hoja, M.-R., Wilbertz, J., Nordqvist, K., Hoog, C. (2002). Female Germ Cell Aneuploidy and Embryo Death in Mice Lacking the Meiosis-Specific Protein SCP3. Science 296: 1115-1118 [Abstract] [Full Text]  
  • Hirano, T. (2002). The ABCs of SMC proteins: two-armed ATPases for chromosome condensation, cohesion, and repair. Genes Dev. 16: 399-414 [Full Text]