Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis

Journal of Cell Biology

Volumn 173, Issue 4, 2006, Pages 497-507

  Yang, Fang ^a   De La Fuente, Rabindranath ^a   Leu, N Adrian ^a   Baumann, Claudia ^a   McLaughlin, K John ^a   Wang, P Jeremy ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN SYCP2; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ALLELE; APOPTOSIS; ARTICLE; CROSSING OVER; FEMALE FERTILITY; GENE DISRUPTION; GENE TARGETING; IN VIVO STUDY; MALE FERTILITY; MALE STERILITY; MEIOSIS; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPERMATOCYTE; SYNAPTONEMAL COMPLEX;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME PAIRING; CHROMOSOMES; CONSERVED SEQUENCE; FEMALE; INFERTILITY, FEMALE; INFERTILITY, MALE; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; OOCYTES; PROTEIN STRUCTURE, TERTIARY; SEX CHARACTERISTICS; SEX DIFFERENTIATION; SPERMATOCYTES; SPERMATOGENESIS; SYNAPTONEMAL COMPLEX;

MAMMALIA; SYNAPSIS;

EID: 33646770606     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200603063     Document Type: Article

References (47)

1. Bailis, J.M., and G.S. Roeder. 1998. Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev. 12:3551-3563.
2. Chuma, S., and N. Nakatsuji. 2001. Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev. Biol. 229:468-479.
3. Colaiacovo, M.P., A.J. MacQueen, E. Martinez-Perez, K. McDonald, A. Adamo, A. La Volpe, and A.M. Villeneuve. 2003. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell. 5:463-474.
4. Costa, Y., R. Speed, R. Ollinger, M. Alsheimer, C.A. Semple, P. Gautier, K. Maratou, I. Novak, C. Hoog, R. Benavente, and H.J. Cooke. 2005. Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci. 118:2755-2762.
5. de los Santos, T., and N.M. Hollingsworth. 1999. Red1p, a MEK1-dependent phosphoprotein that physically interacts with Hop1p during meiosis in yeast. J. Biol. Chem. 274:1783-1790.
6. de Vries, F.A., 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. 2005. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19:1376-1389.
7. Dobson, M.J., R.E. Pearlman, A. Karaiskakis, B. Spyropoulos, and P.B. Moens. 1994. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107:2749-2760.
8. Dresser, M.E., and M.J. Moses. 1979. Silver staining of synaptonemal complexes in surface spreads for light and electron microscopy. Exp. Cell Res. 121:416-419.
9. Fawcett, D.W. 1956. The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J. Biophys. Biochem. Cytol. 2:403-406.
10. Friedman, D.B., N.M. Hollingsworth, and B. Byers. 1994. Insertional mutations in the yeast HOP1 gene: evidence for multimeric assembly in meiosis. Genetics. 136:449-464.
11. Heyting, C., A.J. Dietrich, P.B. Moens, R.J. Dettmers, H.H. Offenberg, E.J. Redeker, and A.C. Vink. 1989. Synaptonemal complex proteins. Genome. 31:81-87.
12. Hollingsworth, N.M., and L. Ponte. 1997. Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae. Genetics. 147:33-42.
13. Hunt, P.A., and T.J. Hassold. 2002. Sex matters in meiosis. Science. 296:2181-2183.
14. Kolas, N.K., L. Yuan, C. Hoog, H.H. Heng, E. Marcon, and P.B. Moens. 2004. Male mouse meiotic chromosome cores deficient in structural proteins SYCP3 and SYCP2 align by homology but fail to synapse and have possible impaired specificity of chromatin loop attachment. Cytogenet. Genome Res. 105:182-188.
15. Kolas, N.K., E. Marcon, M.A. Crackower, C. Hoog, J.M. Penninger, B. Spyropoulos, and P.B. Moens. 2005. Mutant meiotic chromosome core components in mice can cause apparent sexual dimorphic endpoints at prophase or X-Y defective male-specific sterility. Chromosoma. 114:92-102.
16. Kouznetsova, A., I. Novak, R. Jessberger, and C. Hoog. 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.
17. Lammers, J.H., H.H. Offenberg, M. van Aalderen, A.C. Vink, A.J. Dietrich, and C. Heyting. 1994. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol. Cell. Biol. 14:1137-1146.
18. Liebe, B., M. Alsheimer, C. Hoog, R. Benavente, and H. Scherthan. 2004. Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell. 15:827-837.
19. Liu, J.G., L. Yuan, E. Brundell, B. Bjorkroth, B. Daneholt, and C. Hoog. 1996. Localization of the N-terminus of SCP1 to the central element of the synaptonemal complex and evidence for direct interactions between the N-termini of SCP1 molecules organized head-to-head. Exp. Cell Res. 226:11-19.
20. MacQueen, A.J., M.P. Colaiacovo, K. McDonald, and A.M. Villeneuve. 2002. Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 16:2428-2442.
21. May, M.J., R.B. Marienfeld, and S. Ghosh. 2002. Characterization of the IκB-kinase NEMO binding domain. J. Biol. Chem. 277:45992-46000.
22. Meuwissen, R.L., H.H. Offenberg, A.J. Dietrich, A. Riesewijk, M. van Iersel, and C. Heyting. 1992. A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11:5091-5100.
23. Moens, P.B., and B. Spyropoulos. 1995. Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma. 104:175-182.
24. Moses, M.J. 1956. Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol. 2:215-218.
25. Moses, M.J. 1969. Structure and function of the synaptonemal complex. Genetics. 61:41-51.
26. Offenberg, H.H., J.A. Schalk, R.L. Meuwissen, M. van Aalderen, H.A. Kester, A.J. Dietrich, and C. Heyting. 1998. SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res. 26:2572-2579.
27. Page, S.L., and R.S. Hawley. 2001. c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev. 15:3130-3143.
28. Page, S.L., and R.S. Hawley. 2004. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20:525-558.
29. Pelttari, J., M.R. Hoja, L. Yuan, J.G. Liu, E. Brundell, P. Moens, S. Santucci-Darmanin, R. Jessberger, J.L. Barbero, C. Heyting, and C. Hoog. 2001. 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. Mol. Cell. Biol. 21:5667-5677.
30. Peters, A.H., A.W. Plug, M.J. van Vugt, and P. de Boer. 1997. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5:66-68.
31. Prieto, I., J.A. Suja, N. Pezzi, L. Kremer, A.C. Martinez, J.S. Rufas, and J.L. Barbero. 2001. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat. Cell Biol. 3:761-766.
32. Roeder, G.S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600-2621.
33. Schalk, J.A., A.J. Dietrich, A.C. Vink, H.H. Offenberg, M. van Aalderen, and C. Heyting. 1998. Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma. 107:540-548.
34. Schalk, J.A., H.H. Offenberg, E. Peters, N.P. Groot, J.M. Hoovers, and C. Heyting. 1999. Isolation and characterization of the human SCP2 cDNA and chromosomal localization of the gene. Mamm. Genome. 10:642-644.
35. Scherthan, H., S. Weich, H. Schwegler, C. Heyting, M. Harle, and T. Cremer. 1996. Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134:1109-1125.
36. Schmekel, K., R.L. Meuwissen, A.J. Dietrich, A.C. Vink, J. van Marle, H. van Veen, and C. Heyting. 1996. Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp. Cell Res. 226:20-30.
37. Smith, A.V., and G.S. Roeder. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136:957-967.
38. Sym, M., J.A. Engebrecht, and G.S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell. 72:365-378.
39. Tarsounas, M., R.E. Pearlman, P.J. Gasser, M.S. Park, and P.B. Moens. 1997. Protein-protein interactions in the synaptonemal complex. Mol. Biol. Cell. 8:1405-1414.
40. Tarsounas, M., T. Morita, R.E. Pearlman, and P.B. Moens. 1999. RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J. Cell Biol. 147:207-220.
41. von Wettstein, D., S.W. Rasmussen, and P.B. Holm. 1984. The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18:331-413.
42. Wang, P.J., and D.C. Page. 2002. Functional substitution for TAFII250 by a retroposed homolog that is expressed in human spermatogenesis. Hum. Mol. Genet. 11:2341-2346.
43. Wang, P.J., J.R. McCarrey, F. Yang, and D.C. Page. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27:422-426.
44. Yang, Z., G.I. Gallicano, Q.C. Yu, and E. Fuchs. 1997. An unexpected localization of basonuclin in the centrosome, mitochondria, and acrosome of developing spermatids. J. Cell Biol. 137:657-669.
45. Yuan, L., J. Pelttari, E. Brundell, B. Bjorkroth, J. Zhao, J.G. Liu, H. Brismar, B. Daneholt, and C. Hoog. 1998. The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J. Cell Biol. 142:331-339.
46. Yuan, L., J.G. Liu, J. Zhao, E. Brundell, B. Daneholt, and C. Hoog. 2000. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol. Cell. 5:73-83.
47. Yuan, L., J.G. Liu, M.R. Hoja, J. Wilbertz, K. Nordqvist, and C. Hoog. 2002. Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science. 296:1115-1118.