The mammalian synaptonemal complex: A scaffold and beyond

Genome Dynamics

Volumn 5, Issue , 2009, Pages 69-80

  Yang, F ^a   Wang, P J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 72; PROTEIN UBC9; RAD51 PROTEIN; NUCLEAR PROTEIN;

CHROMOSOME IDENTIFICATION; CHROMOSOME STRUCTURE; INTERMEDIATE FILAMENT; MAMMAL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SUMOYLATION; SYNAPTONEMAL COMPLEX; ANIMAL; GENETICS; METABOLISM;

MAMMALIA; MUS; SYNAPSIS;

ANIMALS; MAMMALS; NUCLEAR PROTEINS; SYNAPTONEMAL COMPLEX;

EID: 58149198801     PISSN: 16609263     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000166620     Document Type: Review

References (72)

1. Moses MJ: Chromosomal structures in crayfish spermatocytes. J Biophys Biochem Cytol 1956;2:215-218.
2. Fawcett DW: The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Biophys Biochem Cytol 1956;2:403-406.
3. von Wettstein D, Rasmussen SW, Holm PB: The synaptonemal complex in genetic segregation. Annu Rev Genet 1984;18:331-413.
4. Page SL, Hawley RS: The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 2004;20:525-558.
5. Schmekel K, Daneholt B: The central region of the synaptonemal complex revealed in three dimensions. Trends Cell Biol 1995;5:239-242.
6. Moses MJ: Synaptonemal complex karyotyping in spermatocytes of the chinese hamster (Cricetulus griseus). I. Morphology of the autosomal complement in spread preparations. Chromosoma 1977;60:99-125.
7. Moses MJ: Synaptonemal complex karyotyping in spermatocytes of the chinese hamster (Cricetulus griseus). II. Morphology of the XY pair in spread preparations. Chromosoma 1977;60:127-137.
8. Moens PB, Pearlman RE: Chromatin organization at meiosis. Bioessays 1988;9:151-153.
9. Heyting C, Dietrich AJ, Redeker EJ, Vink AC: Structure and composition of synaptonemal complexes, isolated from rat spermatocytes. Eur J Cell Biol 1985;36:307-314.
10. Heyting C, Dietrich AJ, Moens PB, Dettmers RJ, Offenberg HH, Redeker EJ, Vink AC: Synaptonemal complex proteins. Genome 1989;31:81-87.
11. Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, Heyting C: A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 1992;11:5091-5100.
12. Offenberg HH, Schalk JA, Meuwissen RL, van Aalderen M, Kester HA, Dietrich AJ, Heyting C: SCP2: A major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res 1998;26:2572-2579.
13. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB: Synaptonemal complex proteins: Occurrence, epitope mapping and chromosome disjunction. J Cell Sci 1994;107(Pt 10):2749-2760.
14. Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C: 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 1994;14:1137-1146.
15. de Boer E, Heyting C: The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 2006;115:220-234.
16. Revenkova E, Jessberger R: Shaping meiotic prophase chromosomes: Cohesins and synaptonemal complex proteins. Chromosoma 2006;115:235-240.
17. Schalk JA, Dietrich AJ, Vink AC, Offenberg HH, van Aalderen M, Heyting C: Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma 1998;107:540-548.
18. Uhlmann F, Nasmyth K: Cohesion between sister chromatids must be established during DNA replication. Curr Biol 1998;8:1095-1101.
19. Nasmyth K: Disseminating the genome: Joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 2001;35:673-745.
20. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K: A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 1999;98:91-103.
21. Pelttari J, Hoja MR, Yuan L, Liu JG, Brundell E, et al: 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 2001;21:5667-5677.
22. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R: Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 2001;21:6984-6998.
23. Pezzi N, Prieto I, Kremer L, Perez Jurado LA, Valero C, et al: STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 2000;14:581-592.
24. Prieto I, Suja JA, Pezzi N, Kremer L, Martinez-A C, Rufas JS, Barbero JL: Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 2001;3:761-766.
25. Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C: Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 2003;160:657-670.
26. Parra MT, Viera A, Gomez R, Page J, Benavente R, et al: Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 2004;117:1221-1234.
27. Kouznetsova A, Novak I, Jessberger R, Hoog C: SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J Cell Sci 2005;118:2271-2278.
28. Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, et al: Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 2006;126:135-146.
29. Eijpe M, Heyting C, Gross B, Jessberger R: Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes. J Cell Sci 2000;113(Pt 4):673-682.
30. Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC: Positional cloning and characterization of mouse mei8, a disrupted allelle of the meiotic cohesin Rec8. Genesis 2004;40:184-194.
31. Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ: Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 2005;8:949-961.
32. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, et al: Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 2004;6:555-562.
33. Yang F, De La Fuente R, Leu NA, Baumann C, McLaughlin KJ, Wang PJ: Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis. J Cell Biol 2006;173:497-507.
34. Yuan L, Liu JG, Zhao J, Brundell E, Daneholt B, Hoog C: The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol Cell 2000;5:73-83.
35. Tarsounas M, Pearlman RE, Gasser PJ, Park MS, Moens PB: Protein-protein interactions in the synaptonemal complex. Mol Biol Cell 1997;8:1405-1414.
36. Yuan L, Pelttari J, Brundell E, Bjorkroth B, Zhao J, et al: The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J Cell Biol 1998;142:331-339.
37. Baier A, Alsheimer M, Benavente R: Synaptonemal complex protein SYCP3: Conserved polymerization properties among vertebrates. Biochim Biophys Acta 2007;1774:595-602.
38. Tarsounas M, Morita T, Pearlman RE, Moens PB: RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J Cell Biol 1999;147:207-220.
39. Kolas NK, Yuan L, Hoog C, Heng HH, Marcon E, Moens PB: 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 2004;105:182-188.
40. Yuan L, Liu JG, Hoja MR, Wilbertz J, Nordqvist K, Hoog C: Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 2002;296:1115-1118.
41. Liu JG, Yuan L, Brundell E, Bjorkroth B, Daneholt B, Hoog C: 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 1996;226:11-19.
42. Schmekel K, Meuwissen RL, Dietrich AJ, Vink AC, van Marle J, van Veen H, Heyting C: Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp Cell Res 1996;226:20-30.
43. Ollinger R, Alsheimer M, Benavente R: Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell 2005;16:212-217.
44. Sym M, Engebrecht JA, Roeder GS: ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 1993;72:365-378.
45. Page SL, Hawley RS: c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 2001;15:3130-3143.
46. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM: Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 2002;16:2428-2442.
47. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, Villeneuve AM: Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 2003;5:463-474.
48. Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC: The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 2005;19:2488-2500.
49. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, et al: Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 2005;19:1376-1389.
50. Tarsounas M, Pearlman RE, Moens PB: Meiotic activation of rat pachytene spermatocytes with okadaic acid: The behaviour of synaptonemal complex components SYN1/SCP1 and COR1/SCP3. J Cell Sci 1999;112(Pt 4):423-434.
51. Lammers JH, van Aalderen M, Peters AH, van Pelt AA, de Rooij DG, et al: A change in the phosphorylation pattern of the 30000-33000 mr synaptonemal complex proteins of the rat between early and mid-pachytene. Chromosoma 1995;104:154-163.
52. Solari AJ, Moses MJ: The structure of the central region in the synaptonemal complexes of hamster and cricket spermatocytes. J Cell Biol 1973;56:145-152.
53. Costa Y, Speed R, Ollinger R, Alsheimer M, Semple CA, et al: Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J Cell Sci 2005;118:2755-2762.
54. Hamer G, Gell K, Kouznetsova A, Novak I, Benavente R, Hoog C: Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex. J Cell Sci 2006;119:4025-4032.
55. Wang PJ, McCarrey JR, Yang F, Page DC: An abundance of X-linked genes expressed in spermatogonia. Nat Genet 2001;27:422-426.
56. Bolcun-Filas E, Costa Y, Speed R, Taggart M, Benavente R, De Rooij DG, Cooke HJ: SYCE2 is required for synaptonemal complex assembly, double strand break repair, and homologous recombination. J Cell Biol 2007;176:741-747.
57. Allen JW, Dix DJ, Collins BW, Merrick BA, He C, et al: HSP70-2 is part of the synaptonemal complex in mouse and hamster spermatocytes. Chromosoma 1996;104:414-421.
58. Dix DJ, Allen JW, Collins BW, Poorman-Allen P, Mori C, et al: HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes. Development 1997;124:4595-4603.
59. Zhu D, Dix DJ, Eddy EM: HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes. Development 1997;124:3007-3014.
60. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, et al: Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 2003;300:1291-1295.
61. Cheng CH, Lo YH, Liang SS, Ti SC, Lin FM, et al: SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev 2006;20:2067-2081.
62. Hooker GW, Roeder GS: A role for SUMO in meiotic chromosome synapsis. Curr Biol 2006;16:1238-1243.
63. Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, et al: Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc Natl Acad Sci USA 1996;93:2958-2963.
64. Koshiyama A, Hamada FN, Namekawa SH, Iwabata K, Sugawara H, et al: Sumoylation of a meiosis-specific RecA homolog, Lim15/Dmc1, via interaction with the small ubiquitin-related modifier (SUMO)-conjugating enzyme Ubc9. FEBS J 2006;273:4003-4012.
65. Yamaguchi YL, Tanaka SS, Yasuda K, Matsui Y, Tam PP: Stage-specific Importin13 activity influences meiosis of germ cells in the mouse. Dev Biol 2006;297:350-360.
66. Wang H, Hoog C: Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes. J Cell Biol 2006;173:485-495.
67. Hassold T, Hunt P: To err (meiotically) is human: The genesis of human aneuploidy. Nat Rev Genet 2001;2:280-291.
68. Kouznetsova A, Lister L, Nordenskjold M, Herbert M, Hoog C: Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat Genet 2007;39:966-968.
69. Miyamoto T, Hasuike S, Yogev L, Maduro MR, Ishikawa M, Westphal H, Lamb DJ: Azoospermia in patients heterozygous for a mutation in SYCP3. Lancet 2003;362:1714-1719.
70. Neumann F, Wagner C, Preuss KD, Kubuschok B, Schormann C, Stevanovic S, Pfreundschuh M: Identification of an epitope derived from the cancer testis antigen HOM-TES-14/SCP1 and presented by dendritic cells to circulating CD4+ T cells. Blood 2005;106:3105-3113.
71. Daugaard M, Jaattela M, Rohde M: Hsp70-2 is required for tumor cell growth and survival. Cell Cycle 2005;4:877-880.
72. Rohde M, Daugaard M, Jensen MH, Helin K, Nylandsted J, Jaattela M: Members of the heat-shock protein 70 family promote cancer cell growth by distinct mechanisms. Genes Dev 2005;19:570-582.