Journal of Cell Science, Vol 107, Issue 10 2749-2760, Copyright © 1994 by Company of Biologists

JOURNAL ARTICLES

Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction

MJ Dobson, RE Pearlman, A Karaiskakis, B Spyropoulos and PB Moens
Department of Biology, York University, Downsview, Ontario, Canada.

We have used polyclonal antibodies against fusion proteins produced from cDNA fragments of a meiotic chromosome core protein, Cor1, and a protein present only in the synapsed portions of the cores, Syn1, to detect the occurrence and the locations of these proteins in rodent meiotic prophase chromosomes. The 234 amino acid Cor1 protein is present in early unpaired cores, in the lateral domains of the synaptonemal complex and in the chromosome cores when they separate at diplotene. A novel observation showed the presence of Cor1 axial to the metaphase I chromosomes and substantial amounts of Cor1 in association with pairs of sister centromeres. The centromere-associated Cor1 protein becomes dissociated from the centromeres at anaphase II and it is not found in mitotic metaphase centromeres. The extended presence of Cor1 suggests that it may have a role in chromosome disjunction by fastening chiasmata at metaphase I and by joining sister kinetochores, which ensures co-segregation at anaphase I. Two-colour immunofluorescence of Cor1 and Syn1 demonstrates that synapsis between homologous cores is initiated at few sites but advances rapidly relative to the establishment of new initiation sites. If the rapid advance of synapsis deters additional initiation sites between pairs of homologues, it may provide a mechanism for positive recombination interference. Immunogold epitope mapping of antibodies to four Syn1 fusion proteins places the amino terminus of Syn1 towards the centre of the synaptonemal complex while the carboxyl terminus extends well into the lateral domain of the synaptonemal complex. The Syn1 fusion proteins have a non-specific DNA binding capacity. Immunogold labelling of Cor1 antigens indicates that the lateral domain of the synaptonemal complex is about twice as wide as the apparent width of lateral elements when stained with electron-dense metal ions. Electron microscopy of shadow-cast surface-spread SCs confirms the greater width of the lateral domain. The implication of these dimensions is that the proteins that comprise the synaptic domain overlap with the protein constituents of the lateral domains of the synaptonemal complex more than was apparent from earlier observations. This arrangement suggests that direct interactions might be expected between some of the synaptonemal complex proteins.
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				M Eijpe, C Heyting, B Gross, and R Jessberger Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes J. Cell Sci., January 2, 2000; 113(4): 673 - 682. [Abstract] [PDF]

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				M Tarsounas, R. Pearlman, and P. Moens Meiotic activation of rat pachytene spermatocytes with okadaic acid: the behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3 J. Cell Sci., January 2, 1999; 112(4): 423 - 434. [Abstract] [PDF]

				D. Escalier, B. Allenet, A. Badrichani, and H.-J. Garchon High Level Expression of the Xlr Nuclear Protein in Immature Thymocytes and Colocalization with the Matrix-Associated Region-Binding SATB1 Protein J. Immunol., January 1, 1999; 162(1): 292 - 298. [Abstract] [Full Text] [PDF]

				M. L. Watson, A. R. Zinn, N. Inoue, K. D. Hess, J. Cobb, M. A. Handel, R. Halaban, C. C. Duchene, G. M. Albright, and R. W. Moreadith Identification of morc (microrchidia), a mutation that results in arrest of spermatogenesis at an early meiotic stage in the mouse PNAS, November 24, 1998; 95(24): 14361 - 14366. [Abstract] [Full Text] [PDF]

				Y. Kimura,, H. Tateno,, M. A. Handel,, and R. Yanagimachi Factors Affecting Meiotic and Developmental Competence of Primary Spermatocyte Nuclei Injected into Mouse Oocytes Biol Reprod, October 1, 1998; 59(4): 871 - 877. [Abstract] [Full Text]

				R. Freire, J. R. Murguía, M. Tarsounas, N. F. Lowndes, P. B. Moens, and S. P. Jackson Human and mouse homologs of Schizosaccharomyces pombe rad1+ and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis Genes & Dev., August 15, 1998; 12(16): 2560 - 2573. [Abstract] [Full Text]

				L. Yuan, J. Pelttari, E. Brundell, B. Bjorkroth, J. Zhao, J.-G. Liu, H. Brismar, B. Daneholt, and C. Hoog The Synaptonemal Complex Protein SCP3 Can Form Multistranded, Cross-striated Fibers In Vivo J. Cell Biol., July 27, 1998; 142(2): 331 - 339. [Abstract] [Full Text] [PDF]

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				C Barlow, M Liyanage, P. Moens, M Tarsounas, K Nagashima, K Brown, S Rottinghaus, S. Jackson, D Tagle, T Ried, et al. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I Development, January 10, 1998; 125(20): 4007 - 4017. [Abstract] [PDF]

				A. Plug, A. Peters, K. Keegan, M. Hoekstra, P de Boer, and T Ashley Changes in protein composition of meiotic nodules during mammalian meiosis J. Cell Sci., January 2, 1998; 111(4): 413 - 423. [Abstract] [PDF]

				J. F. Marko and E. D. Siggia Polymer Models of Meiotic and Mitotic Chromosomes Mol. Biol. Cell, November 1, 1997; 8(11): 2217 - 2231. [Abstract] [Full Text]

				G. S. Roeder Meiotic chromosomes: it takes two to tango Genes & Dev., October 15, 1997; 11(20): 2600 - 2621. [Full Text] [PDF]

				A. V. Smith and G. S. Roeder The Yeast Red1 Protein Localizes to the Cores of Meiotic Chromosomes J. Cell Biol., March 10, 1997; 136(5): 957 - 967. [Abstract] [Full Text] [PDF]

				A. W. Plug, C. A. Clairmont, E. Sapi, T. Ashley, and J. B. Sweasy Evidence for a role for DNA polymerase beta  in mammalian meiosis PNAS, February 18, 1997; 94(4): 1327 - 1331. [Abstract] [Full Text] [PDF]

				D. Dix, J. Allen, B. Collins, P Poorman-Allen, C Mori, D. Blizard, P. Brown, E. Goulding, B. Strong, and E. Eddy HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes Development, January 11, 1997; 124(22): 4595 - 4603. [Abstract] [PDF]

				D Zhu, D. Dix, and E. Eddy HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes Development, January 8, 1997; 124(15): 3007 - 3014. [Abstract] [PDF]

				Y Xu, T Ashley, E E Brainerd, R T Bronson, M S Meyn, and D Baltimore Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes & Dev., October 1, 1996; 10(19): 2411 - 2422. [Abstract] [PDF]

				K S Keegan, D A Holtzman, A W Plug, E R Christenson, E E Brainerd, G Flaggs, N J Bentley, E M Taylor, M S Meyn, S B Moss, et al. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes & Dev., October 1, 1996; 10(19): 2423 - 2437. [Abstract] [PDF]