Homologous Chromosome Pairing and Synapsis during Oogenesis

Oogenesis: The Universal Process

Volumn , Issue , 2010, Pages 115-140

  Mlynarczyk Evans, Susanna ^a   Villeneuve, Anne ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Bouquet; Chromosome dynamics; Homolog recognition; HORMA domain; KASH domain; Meiosis; SUN domain; Synaptonemal complex

Indexed keywords

EID: 84886028910     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9780470687970.ch5     Document Type: Chapter

References (135)

1. Alani, E., Padmore, R. and Kleckner, N. (1990) Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell, 61, 419-436.
2. Aravind, L. and Koonin, E.V. (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem. Sci., 23, 284-286.
3. Baker, S.M., Plug, A.W., Prolla, T.A. et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet., 13, 336-342.
4. Bannister, L.A., Reinholdt, L.G., Munroe, R.J. and Schimenti, J.C. (2004) Positional cloning and characterization of mouse mei8, a disrupted allele of the meiotic cohesin Rec8. Genesis, 40, 184-194.
5. Barchi, M., Mahadevaiah, S., Di Giacomo, M. et al. (2005) Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell Biol., 25, 7203-7215.
6. Barlow, C., Liyanage, M., Moens, P.B. et al. (1998) Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development, 125, 4007-4017.
7. Baudat, F. and de Massy, B. (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res., 15, 565-577.
8. Baudat, F., Manova, K., Yuen, J.P. et al. (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell, 6, 989-998.
9. Bhalla, N. and Dernburg, A.F. (2005)Aconserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science, 310, 1683-1686.
10. Bickel, S.E., Orr-Weaver, T.L. and Balicky, E.M. (2002) The sister-chromatid cohesion protein ORD is required for chiasma maintenance in Drosophila oocytes. Curr. Biol., 12, 925-929.
11. Bolcun-Filas, E., Costa, Y., Speed, R. et al. (2007) SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J. Cell Biol., 176, 741-747.
12. Bolcun-Filas, E., Speed, R., Taggart, M. et al. (2009) Mutation of the mouse Syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLoS Genet., 5, e1000393.
13. Chan, R.C., Chan, A., Jeon, M. et al. (2003) Chromosome cohesion is regulated by a clock gene paralogue TIM-1. Nature, 423, 1002-1009.
14. Chikashige, Y., Ding, D.Q., Funabiki, H. et al. (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science, 264, 270-273.
15. Chikashige, Y., Haraguchi, T. and Hiraoka, Y. (2007) Another way to move chromosomes. Chromosoma, 116, 497-505.
16. Cohen, P.E., Pollack, S.E. and Pollard, J.W. (2006) Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr. Rev., 27, 398-426.
17. Colaiacovo, M.P., Stanfield, G.M., Reddy, K.C. et al. (2002) A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics, 162, 113-128.
18. Colaiacovo, M.P., MacQueen, A.J., Martinez-Perez, E. et al. (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.
19. Conrad, M.N., Lee, C.Y., Chao, G. et al. (2008) Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell, 133, 1175-1187.
20. Costa, Y., Speed, R., Ollinger, R. et al. (2005) Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci., 118, 2755-2762.
21. Couteau, F., Nabeshima, K., Villeneuve, A. and Zetka, M. (2004) A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr. Biol., 14, 585-592.
22. Couteau, F. and Zetka, M. (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev., 19, 2744-2756.
23. Dernburg, A.F., McDonald, K., Moulder,G. et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell, 94, 387-398.
24. Di Giacomo, M., Barchi, M., Baudat, F. et al. (2005) Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc. Natl. Acad. Sci. USA, 102, 737-742.
25. Ding, D.Q., Yamamoto, A., Haraguchi, T. and Hiraoka, Y. (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev. Cell, 6, 329-341.
26. Ding, X., Xu, R.,Yu, J. et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell, 12, 863-872.
27. Dobson, M.J., Pearlman, R.E., Karaiskakis, A. et al. (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci., 107(10),2749-2760.
28. Edelmann,W., Cohen, P.E., Kane, M. et al. (1996) Meiotic pachytene arrest in MLH1-deficient mice. Cell, 85, 1125-1134.
29. Edelmann, W., Cohen, P.E., Kneitz, B. et al. (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet., 21, 123-127.
30. Fukuda, T., Daniel, K., Wojtasz, L. et al. (2009) A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp. Cell Res., in press.
31. Fung, J.C., Marshall,W.F., Dernburg, A. et al. (1998) Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol., 141, 5-20.
32. Gartner, A., Milstein, S., Ahmed, S. et al. (2000) A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell, 5, 435-443.
33. Ghafari, F., Gutierrez, C.G. and Hartshorne, G.M. (2007) Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one. BMC Dev. Biol., 7, 87.
34. Gillies, C.B. (1974) The nature and extent of synaptonemal complex formation in haploid barley. Chromosoma, 48, 441-453.
35. Giroux, C.N., Dresser, M.E. and Tiano, H.F. (1989) Genetic control of chromosome synapsis in yeast meiosis. Genome, 31, 88-94.
36. Goldstein, P. and Slaton, D.E. (1982) The synaptonemal complexes of Caenorhabditis elegans: comparison of wild-type and mutant strains and pachytene karyotype analysis of wild-type. Chromosoma, 84, 585-597.
37. Gong,W.J., McKim, K.S. and Hawley, R.S. (2005) All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote. PLoS Genet., 1, e67.
38. Goodyer,W., Kaitna, S., Couteau, F. et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell, 14, 263-274.
39. Gorbsky, G.J., Chen, R.H. and Murray, A.W. (1998) Microinjection of antibody to Mad2 protein into mammalian cells in mitosis induces premature anaphase. J. Cell Biol., 141, 1193-1205.
40. Grant, B. and Hirsh, D. (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell, 10, 4311-4326.
41. Gumienny, T.L., Lambie, E., Hartwieg, E. et al. (1999) Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development, 126, 1011-1022.
42. Hamer, G., Gell, K.,Kouznetsova, A. et al. (2006) Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J. Cell Sci., 119, 4025-4032.
43. Hamer, G., Wang, H., Bolcun-Filas, E. et al. (2008) Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J. Cell Sci., 121, 2445-2451.
44. Harper, L., Golubovskaya, I. and Cande, W.Z. (2004) A bouquet of chromosomes. J. Cell Sci., 117, 4025-4032.
45. Hassold, T. and Hunt, P. (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet., 2, 280-291.
46. Hawley, R.S. (1980) Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. Genetics, 94, 625-646.
47. Hayashi, M., Chin, G.M. and Villeneuve, A.M. (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet., 3, e191.
48. Heidmann, D., Horn, S., Heidmann, S. et al. (2004) The Drosophila meiotic kleisin C(2)M functions before the meiotic divisions. Chromosoma, 113, 177-187.
49. Herman, R.K. and Kari, C.K. (1989) Recombination between small X chromosome duplications and the X chromosome in Caenorhabditis elegans. Genetics, 121, 723-737.
50. Herman, R.K., Kari, C.K. and Hartman, P.S. (1982) Dominant X-chromosome nondisjunction mutants of Caenorhabditis elegans. Genetics, 102, 379-400.
51. Hiraoka, Y., Dernburg, A.F., Parmelee, S.J. et al. (1993) The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis. J. Cell Biol., 120, 591-600.
52. Hollingsworth, N.M., Goetsch, L. and Byers, B. (1990) The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell, 61, 73-84.
53. Jeffress, J.K., Page, S.L., Royer, S.K. et al. (2007) The formation of the central element of the synaptonemal complex may occur by multiple mechanisms: the roles of the N- and C-terminal domains of the Drosophila C(3)G protein in mediating synapsis and recombination. Genetics, 177, 2445-2456.
54. Joyce, E.F. and McKim, K.S. (2009) Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics, 181, 39-51.
55. Keeney, S. (2001) Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol., 52, 1-53.
56. Khetani, R.S. and Bickel, S.E. (2007) Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J. Cell Sci., 120, 3123-3137.
57. Kneitz, B., Cohen, P.E., Avdievich, E. et al. (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes. Dev., 14, 1085-1097.
58. Kosaka, H., Shinohara, M. and Shinohara, A. (2008) Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet., 4, e1000196.
59. Koszul, R., Kim, K.P., Prentiss, M. et al. (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell, 133, 1188-1201.
60. Lammers, J.H., Offenberg, H.H., van Aalderen, M. et al. (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyteregulated genes. Mol. Cell Biol., 14, 1137-1146.
61. Lee, J.Y. and Orr-Weaver, T.L. (2001) The molecular basis of sister-chromatid cohesion. Annu. Rev. Cell Dev. Biol., 17, 753-777.
62. Li, X.C. and Schimenti, J.C. (2007) Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet., 3, e130.
63. Liebe, B., Alsheimer, M., Hoog, C. et al. (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell, 15, 827-837.
64. Liebe, B., Petukhova, G., Barchi, M. et al. (2006) Mutations that affect meiosis in male mice influence the dynamics of the mid-preleptotene and bouquet stages. Exp. Cell Res., 312, 3768-3781.
65. Lipkin, S.M., Moens, P.B., Wang, V. et al. (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet., 31, 385-390.
66. Loidl, J. (1990) The initiation of meiotic chromosome pairing: the cytological view. Genome, 33, 759-778.
67. Loidl, J., Nairz, K. and Klein, F. (1991) Meiotic chromosome synapsis in a haploid yeast. Chromosoma, 100, 221-228.
68. MacQueen, A.J., Colaiacovo, M.P., McDonald, K. and Villeneuve, A.M. (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes. Dev., 16, 2428-2442.
69. MacQueen, A.J., Phillips, C.M., Bhalla, N. et al. (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell, 123, 1037-1050.
70. MacQueen, A.J. and Villeneuve, A.M. (2001) Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes. Dev., 15, 1674-1687.
71. Mahadevaiah, S.K., Turner, J.M., Baudat, F. et al. (2001) RecombinationalDNAdouble-strand breaks in mice precede synapsis. Nat. Genet., 27, 271-276.
72. Malone, C.J., Misner, L., Le Bot, N. et al. (2003) The C. elegans hook protein, ZYG-12, mediates the essential attachment between the centrosome and nucleus. Cell, 115, 825-836.
73. Manheim, E.A. and McKim, K.S. (2003) The synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila. Curr. Biol., 13, 276-285.
74. Mark, M., Jacobs, H., Oulad-Abdelghani, M. et al. (2008) STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation. J. Cell Sci., 121, 3233-3242.
75. Martinez-Perez, E., Schvarzstein, M., Barroso, C. et al. (2008) Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev., 22, 2886-2901.
76. Martinez-Perez, E. and Villeneuve, A.M. (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes. Dev., 19, 2727-2743.
77. McKee, B.D. (2009) Homolog pairing and segregation in Drosophila meiosis. Genome Dyn., 5, 56-68.
78. McKim, K.S., Green-Marroquin, B.L., Sekelsky, J.J. et al. (1998) Meiotic synapsis in the absence of recombination. Science, 279, 876-878.
79. McKim, K.S. and Hayashi-Hagihara, A. (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes. Dev., 12, 2932-2942.
80. McKim, K.S., Howell, A.M. and Rose, A.M. (1988) The effects of translocations on recombination frequency in Caenorhabditis elegans. Genetics, 120, 987-1001.
81. McKim, K.S., Peters, K. and Rose, A.M. (1993) Two types of sites required for meiotic chromosome pairing in Caenorhabditis elegans. Genetics, 134, 749-768.
82. Meuwissen, R.L., Offenberg, H.H., Dietrich, A.J. et al. (1992)Acoiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J., 11, 5091-5100.
83. Miyazaki,W.Y. and Orr-Weaver,T.L. (1992) Sister-chromatid misbehavior in Drosophila ord mutants. Genetics, 132, 1047-1061.
84. Moses, M.J. (1956) Chromosomal structures in crayfish spermatocytes. J. Biophys. Biochem. Cytol., 2, 215-218.
85. Nabeshima, K.,Villeneuve, A.M. and Colaiacovo, M.P. (2005) Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol., 168, 683-689.
86. Nabeshima, K., Villeneuve, A.M. and Hillers, K.J. (2004) Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics, 168, 1275-1292.
87. Novak, I.,Wang, H., Revenkova,E. et al. (2008) Cohesin Smc1beta determines meiotic chromatin axis loop organization. J. Cell Biol., 180, 83-90.
88. Odorisio, T., Rodriguez, T.A., Evans, E.P. et al. (1998) The meiotic checkpoint monitoring synapsis eliminates spermatocytes via p53-independent apoptosis. Nat. Genet., 18, 257-261.
89. Offenberg, H.H., Schalk, J.A., Meuwissen, R.L. et al. (1998) SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res., 26, 2572-2579.
90. Ollinger, R., Alsheimer,M. and Benavente, R. (2005) Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol. Biol. Cell, 16, 212-217.
91. Page, S.L. and Hawley, R.S. (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes. Dev., 15, 3130-3143.
92. Page, S.L., Khetani, R.S., Lake, C.M. et al. (2008) Corona is required for higher-order assembly of transverse filaments into full-length synaptonemal complex in Drosophila oocytes. PLoS Genet., 4, e1000194.
93. Pasierbek, P., Fodermayr, M., Jantsch, V. et al. (2003) The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. Exp. Cell Res., 289, 245-255.
94. Pasierbek, P., Jantsch, M., Melcher, M. et al. (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes. Dev., 15, 1349-1360.
95. Penkner, A., Tang, L., Novatchkova, M. et al. (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev. Cell, 12, 873-885.
96. Pfeifer, C., Scherthan, H. and Thomsen, P.D. (2003) Sex-specific telomere redistribution and synapsis initiation in cattle oogenesis. Dev. Biol., 255, 206-215.
97. Phillips, C.M. and Dernburg, A.F. (2006)Afamily of zinc-finger proteins is required for chromosomespecific pairing and synapsis during meiosis in C. elegans. Dev. Cell, 11, 817-829.
98. Phillips, C.M., Meng, X., Zhang, L. et al. (2009) Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat. Cell Biol., 11, 934-942.
99. Phillips, C.M.,Wong, C., Bhalla, N. et al. (2005) HIM-8 binds to theXchromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell, 123, 1051-1063.
100. Pittman, D.L.,Cobb, J., Schimenti,K.J. et al. (1998)Meiotic prophase arrestwith failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell, 1, 697-705.
101. Prieto, I., Suja, J.A., Pezzi, N. et al. (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat. Cell Biol., 3, 761-766.
102. Prieto, I., Tease, C., Pezzi, N. et al. (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res., 12, 197-213.
103. Revenkova, E., Eijpe, M., Heyting, C. et al. (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat. Cell Biol., 6, 555-562.
104. Revenkova, E. and Jessberger, R. (2006) Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma, 115, 235-240.
105. Roig, I., Liebe, B., Egozcue, J. et al. (2004) Female-specific features of recombinational doublestranded DNA repair in relation to synapsis and telomere dynamics in human oocytes. Chromosoma, 113, 22-33.
106. Romanienko, P.J. and Camerini-Otero, R.D. (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell, 6, 975-987.
107. Scherthan, H. (2001) A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol., 2, 621-627.
108. Scherthan, H., Weich, S., Schwegler, H. et al. (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.
109. Schmekel, K. and Daneholt, B. (1995) The central region of the synaptonemal complex revealed in three dimensions. Trends Cell Biol., 5, 239-242.
110. Severson, A.F., Ling, L., van Zuylen, V. and Meyer, B.J. (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev., 23, 1763-1778.
111. Sherizen, D., Jang, J.K., Bhagat, R. et al. (2005) Meiotic recombination in Drosophila females depends on chromosome continuity between genetically defined boundaries. Genetics, 169, 767-781.
112. Smolikov, S., Eizinger, A., Schild-Prufert, K. et al. (2007) SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics, 176, 2015-2025.
113. Smolikov, S., Schild-Prufert, K. and Colaiacovo, M.P. (2009) A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet., 5, e1000669.
114. Staeva-Vieira, E.,Yoo, S. and Lehmann, R. (2003) An essential role of DmRad51/SpnA inDNArepair and meiotic checkpoint control. EMBO J., 22, 5863-5874.
115. Sym, M., Engebrecht, J.A. and Roeder, G.S. (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell, 72, 365-378.
116. Tankimanova, M., Hulten, M.A. and Tease, C. (2004) The initiation of homologous chromosome synapsis in mouse fetal oocytes is not directly driven by centromere and telomere clustering in the bouquet. Cytogenet. Genome Res., 105, 172-181.
117. Trelles-Sticken, E., Adelfalk, C., Loidl, J. and Scherthan, H. (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J. Cell Biol., 170, 213-223.
118. Trelles-Sticken, E., Dresser, M.E. and Scherthan, H. (2000) Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol., 151, 95-106.
119. Tsubouchi, T., Macqueen, A.J. and Roeder, G.S. (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes. Dev., 22, 3217-3226.
120. Tsubouchi, T. and Roeder, G.S. (2005) A synaptonemal complex protein promotes homologyindependent centromere coupling. Science, 308, 870-873.
121. Vazquez, J., Belmont, A.S. and Sedat, J.W. (2002) The dynamics of homologous chromosome pairing during male Drosophila meiosis. Curr. Biol., 12, 1473-1483.
122. Villeneuve, A.M. (1994) A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics, 136, 887-902.
123. de Vries, F.A., de Boer, E., van den Bosch, M. et al. (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev., 19, 1376-1389.
124. de Vries, S.S., Baart, E.B., Dekker, M. et al. (1999) Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev., 13, 523-531.
125. Wanat, J.J., Kim, K.P., Koszul, R. et al. (2008) Csm4, in collaboration with Ndj1, mediates telomereled chromosome dynamics and recombination during yeast meiosis. PLoS Genet., 4, e1000188.
126. Webber, H.A., Howard, L. and Bickel, S.E. (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. In. J. Cell Biol., 164, 819-829.
127. Wojtasz, L., Daniel, K., Roig, I. et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet., 5, e1000702.
128. Wolke, U., Jezuit, E.A. and Priess, J.R. (2007) Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development, 134, 2227-2236.
129. Xu, H., Beasley, M.D.,Warren,W.D. et al. (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev. Cell, 8, 949-961.
130. Yang, F., De La Fuente, R., Leu, N.A. et al. (2006) Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J. Cell Biol., 173, 497-507.
131. Yoshida, K., Kondoh, G., Matsuda, Y. et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell, 1, 707-718.
132. Yuan, L., Liu, J.G., Hoja, M.R. et al. (2002) Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science, 296, 1115-1118.
133. Yuan, L., Liu, J.G., Zhao, J. et al. (2000) The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol. Cell, 5, 73-83.
134. Zetka, M.C., Kawasaki, I., Strome, S. and Muller, F. (1999) Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes. Dev., 13, 2258-2270.
135. Zickler, D. and Kleckner, N. (1998) The leptotene-zygotene transition of meiosis. Annu. Rev. Genet., 32, 619-697.