Synaptonemal complexes: Structure and function

Current Opinion in Cell Biology

Volumn 8, Issue 3, 1996, Pages 389-396

  Heyting, Christa ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN;

CHROMATIN STRUCTURE; CHROMOSOME CHIASM; CHROMOSOME CONDENSATION; CHROMOSOME PAIRING; CROSSING OVER; GENETIC RECOMBINATION; MEIOSIS; PRIORITY JOURNAL; PROPHASE; REVIEW; SISTER CHROMATID; SYNAPTONEMAL COMPLEX;

EID: 0029980813     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(96)80015-9     Document Type: Article

References (64)

1. Von Wettstein D, Rasmussen SW, Holm PB: The synaptonemal complex in genetic segregation. Annu Rev Genet 1984, 18:331-413.
2. Moses MJ: Chromosomal structures in crayfish spermatocytes. J Biophys Biochem Cytol 1956, 2:215-218.
3. Fawcett DW: The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Biophys Biochem Cytol 1956, 2:403-406.
4. Loidl J: Cytological aspects of meiotic recombination. Experientia 1994, 50:285-294. This review considers the vast amount of cytological investigations of SCs in relation to the recent fluorescent in situ hybridization studies and the analyses of meiotic recombination at the DNA level.
5. Maguire MP: Synaptic initiation and extension as prerequisites for crossing over. Genetics 1974, 45:11-28.
6. Hawley RS, Arbel T: Yeast genetics and the fall of the classical view of meiosis. Cell 1993, 72:301-303.
7. Schmekel K, Skoglund U, Daneholt B: The three-dimensional structure of the central region in a synaptonemal complex a comparison between rat and two insect species, Drosophila melanogaster and Blaps cribrosa. Chromosoma 1993, 102:682-692.
8. Schmekel K, Wahrman J, Skoglund U, Daneholt B: The central region of the synaptonemal complex in Blaps cribrosa studied by electron microscope tomography. Chromosoma 1993, 102:669-681.
9. Schmekel K, Daneholt B: The central region of the synaptonemal complex revealed in three dimensions. Trends Cell Biol 1995, 5:239-242. A detailed overview of what is known about the ultrastructure and composition of the central region of SCs.
10. Kohli J, Baehler J: Homologous recombination in fission yeast: absence of crossover interference and synaptonemal complex. Experientia 1994, 50:295-306. A concise summary of the significance of fission yeast (S. pombe) for meiosis research. S. pombe is an exceptional eukaryotic species in that it does not assemble SCs, nor does it display cross-over interference.
11. Egel-Mitani M, Olson LW, Egel R: Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 1982, 97:179-187.
12. Baehler J, Wyler T, Loidl J, Kohli J: Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J Cell Biol 1993, 121:241-256.
13. Heyting C, Dietrich AJJ, Moens PB, Dettmers RJ, Offenberg HH, Redeker EJW, Vink ACG: Synaptonemal complex proteins. Genome 1989, 31:81-87.
14. Anderson MK, Stack SM, Todd RJ, Ellis RP: A monoclonal antibody to lateral element proteins in synaptonemal complexes of Lilium longoflorum. Chromosoma 1994, 103:357-367.
15. Roeder GS: Sex and the single cell: meiosis in yeast. Proc Natl Acad Sci USA 1995, 92:10450-10456. This review is a guide through the complex and extensive recent literature about meiosis research in yeast.
16. Sym M, Roeder GS: Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol 1995, 128:455-466.
17. Offenberg HH: Identification and characterization of synaptonemal complexes of the rat [PhD Thesis]. Wageningen, The Netherlands: Wageningen Agricultural University; 1993.
18. Lammers JHM, Offenberg HH, Van Aalderen M, Vink ACG, Dietrich AJJ, Heyting C: The gene encoding a major component of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 1994, 14:1137-1146. Cloning of the first gene (cDNA) encoding a component of the lateral elements of SCs.
19. Dobson M, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB: Synaptonemal complex proteins: occurrence, epitope mapping, and chromosome disjunction. J Cell Sci 1994, 107:2749-2760.
20. Meuwissen RLJ, Offenberg HH, Dietrich AJJ, Riesewijk A, Van lersel M, Heyting C: A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 1992, 11:5091-5100.
21. Smith A, Bevavente R: Identification of a structural protein component of rat synaptonemal complexes. Exp Cell Res 1992, 198:291-297.
22. Sym M, Engebrecht J, Roeder GS: ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 1993, 72:365-378.
23. Suzuki M: SPXX, a frequent sequence motif in gene regulatory proteins. J Mol Biol 1989, 207:61-84.
24. Bums N, Grimwade B, RossMacDonald P, Choi EY, Finberg K, Roeder GS, Snyder M: Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev 1994, 8:1087-1105.
25. Bishop D: RecA homologs Dmcl and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 1994, 79:1081-1092. As a result of this immunolocalization study, the RecA-homologous proteins Dmc1p and Rad51p have become candidate components of early RNs.
26. Terasawa M, Shinohara A, Hotta Y, Ogawa H, Ogawa T: Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev 1995, 9:925-934.
27. Klein F, Laroche T, Cardenas ME, Hofmann JFX, Schweizer D, Gasser S: Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast. J Cell Biol 1992, 117:935-948.
28. Moens PB, Earnshaw W: Anti-toposomerase II recognizes meiotic chromosome cores. Chromosoma 1989, 98:317-322.
29. •], presents the intriguing observation that Rad51 p has a different localization relative to SCs in mammals than it does in plants and yeast. In mammals, Rad51p appears to form part of the tripartite segments of SCs.
30. •].
31. Vázquez Nin GH, Flores E, Echeverria OM, Merkert H, Wettstein R, Benavente R: Immunocytochemical localization of DNA in synaptonemal complexes of rat and mouse spermatocytes, and of chick oocytes. Chromosoma 1993, 102:457-463.
32. n and LINE/SINE sequences. Genetics 1992, 130:865-872.
33. Karpova OI, Penkina MV, Dadashev SY, Mil'shina NV, Hernandes J, Radchen ko IV, Bogdanov YF: Primary structure of golden hamster synaptonemal complex DNA. Mol Biol 1995, 3:512-521.
34. Moens PB, Pearlman RE: Telomere and centromere DNA are associated with the cores of meiotic prophase chromosomes. Chromosoma 1990, 100:8-14.
35. Carpenter ATC: The recombination nodule story - seeing what you are looking at Bioessays 1994, 16:69-74. The most up-to-date review of RNs.
36. Sherman JD, Stack SM: Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics 1995, 141:638-708.
37. Zickler D, Moreau P, Huynh AD, Slezec AM: Correlation between pairing initiation sites, recombination nodules and meiotic recombination in Sordaria macrospora. Genetics 1992, 132:135-148.
38. Ashley T: Mammalian meiotic recombination: a reexamination. Hum Genet 1994, 94:587-593. This paper presents convincing examples of discrepancies between the distribution of late RNs and chiasmata along chromosomes in mammals. This suggests that there is an RN-independent pathway of recombination and chiasma formation that is active at meiotic recombinational hotspots in mammals.
39. •].
40. •].
41. Nag DK, Scherthan H, Rockmill B, Bhargava J, Roeder GS: Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 1995, 141:75-86. In this study, homology recognition was analyzed in a variety of yeast meiotic mutants by fluorescence in situ hybridization, and correlated with the formation of heteroduplex DNA.
42. Chikashige Y, Ding DQ, Funabiki H, Haraguchi T, Mashiko S, Yanagida M, Hiraoka Y: Telomere-led premeiotic chromosome movement In fission yeast. Science 1994, 264:270-273. A beautiful description of meiotic telomere and centromere behaviour in fission yeast. The description is helpful for the interpretation of meiotic telomere and centromere behaviour in other organisms.
43. Kohli J: Meiosis - telomeres lead chromosome movement. Curr Biol 1994, 4:724-727.
44. Offenberg HH, Dietrich AJJ, Heyting C: Tissue distribution of two major components of synaptonemal complexes of the rat. Chromosoma 1991, 101:83-91.
45. Heng HHQ, Tsui LC, Moens PB: Organization of heterologous DNA inserts on the mouse meiotic chromosome core. Chromosoma 1994, 103:401-407.
46. Padmore R, Cao L, Kleckner N: Temporal comparison of recombination and synaptonemal complex formation during meiosis In S. cerevisiae. Cell 1991, 66:1239-1266.
47. Dietrich AJJ, Kok E, Offenberg HH, Heyting C, De Boer P, Vink ACG: The sequential appearance of components of synaptonemal complexes during meiosis of the female rat. Genome 1992, 35:492-497.
48. Laemmli UK, Käs E, Poljak L, Adachi Y: Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr Opin Genet Dev 1992, 2:275-285.
49. Maguire MP: Sister chromatid cohesiveness: vital function, obscure mechanism. Biochem Cell Biol 1990, 68:1231-1242.
50. Del Mazo J, Gil-Alberdi L: Multistranded organization of the lateral elements of the synaptonemal complex in the rat and mouse. Cytogenet Cell Genet 1986, 41:219-224.
51. Kleckner N, Padmore R, Bishop DK: Meiotic chromosome metabolism: one view. Cold Spring Harb Symp Quant Biol 1991, 56:729-743.
52. Kleckner N, Weiner BM: Potential advantages of unstable interactions for pairing of chromosomes in meiotic, somatic and premeiotic cells. Cold Spring Harb Symp Quant Biol 1993, 58:553-565.
53. Petes TD, Malone RE, Symington LS: Recombination in yeast In The Molecular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics, edn 8. Edited by Broach JR, Pringle JR, Jones EW. Plainview, New York: Cold Spring Harbor Laboratory Press; 1991:407-521.
54. Lichten M, Goldman ASH: Melotic recombination hotspots. Annu Rev Genet 1995, 29:423-444. A concise review of meiotic recombination hotspots in various organisms.
55. Sears DD, Hieter P, Simchen G: An implanted recombination hot spot stimulates recombination and enhances sister chromatid cohesion of heterologous YACs during yeast meiosis. Genetics 1994, 138:1055-1065.
56. Schwacha A, Kleckner N: Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 1994, 76:51-63. The authors of this article analyzed homologous interactions at a meiotic hotspot of recombination at the DNA level. Recombination intermediates between sister chromatids are distinguished from recombination intermediates between non-sister chromatids.
57. ••] are identified as double Holliday junctions.
58. Rockmill B, Roeder GS: The yeast med1 mutant undergoes both meiotic homolog nondisjunction and precocious separation of sister chromatids. Genetics 1994, 136:65-74.
59. Sym M, Roeder GS: Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 1994, 79:283-292. This is one of the articles that contributed to the switch in opinion about SC function. It demonstrates that, in yeast, a synaptonemal complex protein is required for cross-over interference.
60. Egel R: The synaptonemal complex and the distribution of meiotic recombination events: Trends Genet 1995, 11:206-208. This review summarizes the evidence, obtained from various organisms, that SCs play a role in cross-over interference.
61. Hasenkampf C: The synaptonemal complex - the chaperone of crossing over. Chromosome Res 1996, 4:133-140.
62. Maguire MP: Is the synaptonemal complex a disjunction machine? J Hered 1995, 86:330-340. An up-to-date introduction to the study of synaptonemal complexes.
63. Hollingsworth NM, Goetsch L, Byers B: The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 1990, 61:73-84.
64. Thompson EA, Roeder GS: Expression and DNA sequence of RED1, a gene required for meiosis I chromosome segregation in yeast Mol Gen Genet 1989, 218:293-301.