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

doi:10.1128/MCB.21.16.5667-5677.2001

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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 thegeneration of genetically distinct haploid cells. This has beenattributed in part to a meiosis-specific chromatin-associatedprotein structure, the synaptonemal complex. This complex consistof two parallel axial elements, each one associated with a pairof sister chromatids, and a transverse filament located betweenthe synapsed homologous chromosomes. Recently, a different proteinstructure, the cohesin complex, was shown to be associated withmeiotic 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 mammalianmale meiotic cells, we have analyzed how absence of the axialelement affects early meiotic chromosome behavior. We find thatthe synaptonemal complex protein 3 (SCP3) is a main determinantof axial-element assembly and is required for attachment of thisstructure to meiotic chromosomes, whereas SCP2 helps shape thein vivo structure of the axial element. We also show that formationof a cohesin-containing chromosomal core in meiotic nuclei doesnot require SCP3 or SCP2. Our results also suggest that the cohesincore recruits recombination proteins and promotes synapsis betweenhomologous chromosomes in the absence of an axial element. A modelfor early meiotic chromosome pairing and synapsis isproposed.

^* 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.

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