Chromatin structure contribution to the synaptonemal complex formation

Cellular and Molecular Life Sciences

Volumn 66, Issue 7, 2009, Pages 1198-1208

  Hernandez Hernandez A ^a,b   Vazquez Nin G H ^b   Echeverria O M ^b   Recillas Targa, F ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Chromatin structure; Epigenetic modification; Lateral element associated repeat sequences (LEARS); Meiotic prophase I; Synaptonemal complex

Indexed keywords

DNA; RNA; SCAFFOLD PROTEIN;

CELL CYCLE S PHASE; CELL DIVISION; CHROMATIN; CHROMATIN STRUCTURE; CHROMOSOME; CHROMOSOME PAIRING; DAUGHTER CELL; DEVELOPMENTAL STAGE; DNA METHYLATION; DNA REPLICATION; GAMETE; GENETIC RECOMBINATION; GENETIC VARIABILITY; HAPLOIDY; HUMAN; MEIOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PACHYTENE; PROPHASE; REPRODUCTION; REVIEW; SEQUENCE HOMOLOGY; SYNAPTONEMAL COMPLEX; ZYGOTE;

ANIMALS; CHROMATIN; CHROMOSOMES; DNA METHYLATION; DNA REPLICATION; EPIGENESIS, GENETIC; MEIOSIS; MEIOTIC PROPHASE I; RECOMBINATION, GENETIC; SYNAPTONEMAL COMPLEX;

EID: 63449108874     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8584-2     Document Type: Review

References (73)

1. Zickler, D. and Kleckner, N. (1998) The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-69
2. Felsenfeld, G. and Groudine, M. (2003) Controlling the double helix. Nature 23, 448-453
3. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
4. Vázquez-Nin, G. H., Echeverria, O. M., Ortiz, R., Scassellati, C., Martín, TE., Ubaldo, E. and Fakan, S. (2003) Fine structural cytochemical analysis of homologous chromosome recognition, alignment, and pairing in guinea pig spermatogonia and spermatocytes. Biol. Reproduc. 69, 1362-1370
5. Xu, N., Donohoe, M. E., Silva, S. S. and Lee, J. T. (2007) Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein. Nat. Genet. 39, 1390-1396
6. Wiltshire, T., Park, C. and Handel, M. A. (1998) Chromatin configuration during meiosis I prophase of spermatogenesis. Mol. Reprod. Dev. 49, 70-80
7. Rousseaux, S., Caron, C., Govin, J., Lestrat, C., Faure, A. K. and Khochbin, S. (2005) Establishment of male-specific epigenetic information. Gene. 345, 139-153
8. Webster, K. E., O'Bryan, M. K., Fletcher, S., Crewther, P. E., Aapola, U., Craig, J., Harrison, D. K., Aung, H., Phutikanit, N., Lyle, R., Meachem, S. J., Antonarakis, S. E., de Kretser, D. M., Hedger, M. P., Peterson, P., Caroll B. J. and Scott, H. (2005) Meiotic and epigenetic defects in Dnmt3L-Knockout mouse spermatogenesis. Proc. Natl. Acad. Sci. USA. 102, 4068-4073
9. Peters, A. H. F. M., O'Caroll D., Schertan, H., Mechtler, K., Sauer, S., Schöper, C., Welpoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil S., Doyle, M., Sibilia, M. and Jenuwein, T. (2001) Loss of the Suv39 h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 117, 323-337
10. Kourmouli, N., Jeppesen, P., Mahadevhaiah, S., Burgoyne, P., Wu, R., Gilbert, D. M., Bongiomi, S., Prantera, G., Fanti, L., Pimpinelli, S., Shi, W., Fundeie, R. and Singh, P. B. (2004) Heterochromatin and tri-methylated lysine 20 of histone H4 in animals. J. Cell Sci. 117, 2491-2501
11. Henning, W. (2003) Chromosomal proteins in the spermatogenesis of Drosophila. Chromosoma 11, 489-494
12. Elliott, D. J., Oghene, K., Makarov, G., Makarova, O., Hargreave, T. B., Chandley, A. C., Eperon, I. C. and Cooke, H. J. (1998) Dynamic changes in the subnuclear organization of pre-mRNA splicing proteins and RBM during human germ cell development. J. Cell Sci. 111, 1255-1265
13. Kleckner, N., Zickler, D., Jones, G. H., Dekker, J., Padmore, R., Henle, J. and Hutchinson, J. (2004) A mechanical basis for chromosome function. Proc. Rati. Acad. Sci. USA. 101, 12592-12597
14. Snack, S. M. and Anderson, L. K. (2001) A model for chromosome structure during the mitotic and meiotic cell cycles. Chromosome Res. 9, 175-198
15. Baarends, W. M. and Grootegoed, J. A. (2003) Chromatin dynamics in the male meiotic prophase. Cytogenet. Genome Res. 103, 225-234
16. Dehe, P. M. and Geli, V. (2006) The multiple faces of Set1, Biochem. Cell. Biol. 84, 536-548
17. Vázquez-Rin, G. H. and Echeverría, O. M. (1976) Ultra-structural study on the meiotic prophase nucleus of rat oocytes. Acta Anat. 96, 218-231.
18. Page, S. L. and Hawley R. S. (2004) The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell. Dev. Biol. 20, 525-558
19. Page, S. L. and Hawley, R. S. (2003) Chromosome choreography: the meiotic ballet. Science 301, 785-789
20. Rockmill, B., Sym, M., Scherthan, H. and Roeder, G. S. (1995) Roles for two RecA homologous in promoting chromosome synapsis. Genes Dev. 9, 2684-2695
21. Romanienko, P. J. and Camerini-Otero, R. D. (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell 6, 975-987
22. Bernstein, E. and Hake, S. B. (2006) The nucleosome: a little variation goes a long way. Biochem, Cell Biol, 84, 505-517
23. Roeder, G. S. (1997) Meiotic chromosomes: it takes two to tango. Genes Dev. 11, 2600-2621
24. Stroma, L. and Sjögren, C. (2007) Chromosome segregation and double-strand break repair-a complex connection. Curr. Op. Cell Biol. 19, 344-349
25. Hernández-Hernández, A., Rincón-Arano, H., Recillas-Targa, F., Ortiz, R., Valdes-Quezada, C., Echeverría, O.M., Benavente, R. and Vázquez-Nin, G. H. (2008) Differential distribution and association of repeat DNA sequences in the lateral element of the synaptonemal complex in rat spermatocytes. Chromosoma 117, 77-87
26. Liebe, B., Alsheimer, M., Höög, C., Benavente, R. and Scherthan, H. (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol. Biol. Cell. 15, 827-837
27. Martens, J. H. A., O'sullivan, R. J., Braunschweig, U., Opravil, S., Radolf, M., Steinlein, P. and Jenuwein, T. (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812
28. Tachibana, M., Nozaki, M., Takeda, N. and Shinkai, Y. (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J. 26, 3346-3359
29. Pfeifer, C., Scherthan, H. and Thomsena, P. D. (2003) Sex-specific telomere redistribution and synapsis initiation in cattle oogenesis. Dev. Biol. 255, 206-215
30. Scherthan, H. (2007) Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117-124
31. Pandita, T. K., Hunt, C. R., Sharma, G. G. and Yang, Q. (2007) Regulation of telomere movement by telomere chromatin structure. Cell. Mol. Life Sci. 64, 131-138
32. Ding, X., Xu, R., Yu, J., Xu, T., Zhuang, Y. and Han, M. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell. 12, 863-872
33. Penkner, A., Tang, L., Rovatchkova, M., Ladurner, M., Fridkin, A., Gruenbaum, Y., Schweizer, D., Loidl, J. and Jantsch, V. (2007) The nuclear envelope protein matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev. Cell. 12, 873-85
34. Schmitt, J., Benavente, R., Hodzic, D., Höög, C., Stewart, C. L. and Alsheimer, M. (2007) Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc. Natl. Acad. Sci. USA. 104, 7426-7431
35. Corredor, E. and Naranjo, T. (2007) Effect of colchicine and telocentric chromosome conformation on centromere and telomere dynamics at meiotic prophase I in wheat-rye additions. Chromosome Res. 15, 231-245
36. Misteli, T. (2007) Beyond the sequence: cellular organization and genome function. Cell 128, 787-800
37. Fraser, P. and Bickmore, W. (2007) Nuclear organization of the genome and the potential for gene expression. Nature 447, 413-417
38. Lewis, J. D., Abbott, B. W. and Ausió, J. (2003) A haploid affair: core histone transitions during spermatogenesis. Biochem. Cell. Biol. 81, 131-140
39. Ivanovska, I., Candan, T., Ito, T. and Orr-Weaver, T. L. (2005) A histone code in meiosis: the histone kinase, NHK-1, is required for proper chromosomal architecture in Drosophila oocytes. Gen. Dev. 19, 2571-2582
40. Baarends, W. M., Wassenaar, E., Hoogerbrugge, J. W., van Cappellen, G., Roest, H. P., Vreeburg, J., Ooms, M., Hoeijmakers, J. H. J. and Grootegoed, J. A. (2003) Loss of HR6B ubiquitin-conjugating activity results in damaged synaptonemal complex structure and increased crossing-over frequency during the male meiotic prophase. Mol. Cell. Biol. 23, 1151-1162
41. Baarends, W. M., Wassenaar, E., Hoogerbrugge, J. W., Schoenmakers, S., Sun, S. W. and Grootegoed, J. A. (2007) Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome. J. Cell Sci. 120, 1841-1851
42. Baarends, W. M., Hoogerbrugge, J. W., Roest, H. P., Ooms, M., Vreeburg, J., Hoeijmakers, J. H. J. and Grootegoed, J. A. (1999) Histone ubiquitination and chromatin remolding in mouse spermatogenesis. Dev. Biol. 207, 322-333
43. Rathke, C., Baarends, W. M., Jayaramaiah-Raja, S., Bartkuhn, M., Renkawitz, R. and Renkawitz-Pohl, R. (2007) Transition from a nucleosome-based to a protaminebased chromatin configuration during spermiogenesis in Drosophila. J. Cell Sci. 120, 1689-1700
44. a Ed. Panamericana. Argentina
45. Karpova, O. I., Penkina, M. V., Dadashev, S. Y., Mil'shina, N. V., Hernandes, J., Radchenko, I. V. and Bogdanov, Iu. F. (1995) Features of the primary structure of DNA from the synaptonemal complex of the golden hamster. Mol. Biol. (Mosk) 29, 289-295
46. Karpova, O. I., Safronov, V. V., Zattseva, S. P. and Bogdanov, Y. F. (1989) Some properties of DNA isolated from mouse synaptonemal complexes fraction. Mol. Biol. 23, 571-579
47. n and LINE/SINE sequences. Genetics 130, 865-872
48. Dadashev, S. Ya., Grishaeva, T. M. and Bogdanov, Y. F. (2005) In Silico identification and characterization of meiotic DNA: AluJb possibly participates in the attachment of chromatin loops to synaptonemal complex. Russian. J. Genet. 41, 1419-1424
49. Ortíz, R., Echeverría, O. M., Ubaldo, E., Carlos, A., Scassellati, C. and Vázquez-Nin G. H. (2002) Cytochemical study of the distribution of the RNA and DNA in the synaptonemal complex of guinea-pig and rat spermatocytes. Eur. J. Histochem. 46, 133-142
50. Meuwissen, R. L., Offenberg, H. H., Dietrich, A. J., Riesewijk, A., van Iersel, M. and Heyting, C. (1992) A coiled-coil related protein specific for synapsed region of meiotic prophase chromosomes. EMBO J. 11, 5091-6100
51. Costa, Y., Speed, R., Öllinger, R., Alsheimer, M., Semple, C. A., Gautier, P., Maratou, K., Novak, I., Hoog, C., Benavente, R. and Cooke, H. J. (2005) Two novel proteins recruited by synaptonemal complex protein 1 (SYCP1) are at the centre of meiosis. J. Cell Sci. 118, 2755-2762
52. Yang, F., Gell, K., van der Heijden, G. W., Eckardt, S., Leu, N. A., Page D. C., Benavente, R., Her, C., Höög, C., McLaughlin, K. J. and Wang P. J. (2008) Meiotic failure in male mice lacking an X-linked factor. Genes Dev. 22, 682-691
53. Hamer, G., Gell, K., Kouznetsova, A., Novak, I., Benavente, R., Höög, C. (2006) Characterization of a novel meiosisspecific protein within the central element of the synaptonemal complex. J. Cell Sci. 119, 4025-4032
54. Eijpe, M., Offenberg, H., Jessberger, R., Revenkova, E. and Heyting, C. (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesions SMC1β and SMC3. J. Cell Biol. 160, 657-670
55. Jeffreys, A. J., Holloway, J. K., Kauppi, L., May, C. A., Neumann, R., Slingssy, M. T. and Webb, A. J. (2004) Meiotic recombination hot spots and human DNA diversity. Phil. Trans. R. Soc. Lon. B. 359, 141-152
56. Jeffreys, A. J., Neumann, R., Panayi, M. and Donnelly P. (2005) Human recombination hot spots hidden in regions of strong marker association. Nat. Genet. 37, 601-606
57. Akhmedov, A. T., Frei, C., Tsai-Pflugfelder, M., Kemper, B., Gasser, SM. and Jessberger, R. (1998) Structural maintenance of chromosomes protein C-terminal domains bind preferentially to DNA with secondary structure. J. Biol. Chem. 273, 24088-24094
58. Lobachev, K. S., Rattray, A. and Narayanan, V. (2007) Hairpin-and cruciform-mediated chromosome breakage: causes and consequences in eukaryotic cells. Front. Biosci. 12, 4208-4220
59. Valdeolmillos, A. M., Viera, A., Page, J., Prieto, J., Santos, J. L., Parra, M. T., Heck, M. M. S., Martínez-A, C., Barbero, J. L., Suja, J. A. and Rufas, J. S. (2007) Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers. PLoS Genet. 23, 0204-0215
60. Lammers, J. H. M., Offenberg, H. H., van Aalderen, M., Vink, A. C. G., Dietrich, A. J. J. and Heyting, C. (1994) The gene encoding a major component of the lateral elements of the synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol. Cell Biol. 14, 1137-1146
61. Dobson, M. J., Pearlman, R. E., Karaiskakis, A., Spyropoulos, B. and Moens, P. B. (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107, 2749-2760
62. Offenberg, H. H., Shalk, J. A., Meuwissen, R. L., Van Aaldersen, M., Kester, H. A., Dietrich, A. J. and Heyting, C. (1998) SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res. 26, 2572-2579
63. 63. Revenkova, E., Eijpe, M., Heyting, C., Hodges, C. A., Hunt, P. A., Liebe, B., Scherthan, H. and Jessberger, R. (2004) Cohesin SMC1β is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat. Cell Biol. 6, 555-562
64. Novak, I., Wang, H., Revenkova, E., Jessberger, R., Scherthan, H. and Höög, C. (2008) Cohesin Smc1 beta determines meiotic chromatin axis loop organization. J. Cell Biol. 180, 83-90
65. Pelttari, J., Hoja, M. R., Yuan, L., Liu, J. G., Brundell, E., Moens, P., Santucci-Darmanin, S., Jessberger, R., Barbero, J. L., Heyting, C. and Höög, C. (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, 5667-567
66. Giuffra, E., Törnsten, A., Marklund, S., Bongcam-Rudloff, E., Chardon, P., Kijas, J. M. H., Anderson, S., Archibald, A. L. and Andersson, L. (2002) A large duplication associated with dominant white color in pigs originated by homologous recombination between LINE elements flanking KIT. Mamm. Gen. 13, 569-577
67. De La Fuente, R., Baumann, C., Fan, T., Schmidtmann, A., Dobrinski, I. and Muegge, K. (2006) Lsh is required for meiotic chromosome synapsis and retrotransposon silencing in female germ cells. Nat. Cell Biol. 8, 1448-1454
68. Marcon, E., Babak, T., Chua, G., Hughes, T. and Moens, P. B. (2008) miRNA and piRNA localization in the male mammalian meiotic nucleus. Chromosome Res. 16, 243-260
69. Lippman, Z. and Martienssen, R. (2004) The role of RNA interference in heterochromatic silencing. Nature 431, 364-370
70. Avner, P. and Heard, E. (2001) X-chromosome inactivation: counting, choice and initiation. Nat. Rev. Genet. 2, 59-67
71. Rodríguez-Campos, A. and Azorín, P. (2007) RNA is an integral component of chromatin that contributes to its structural organization. PLoS ONE. 2: e1182
72. Conley, A. B., Millar, W. J. and Jordan, I. K. (2008) Human cis natural antisense transcripts initiated by transposable elements. Trends Genet. 24, 53-56
73. Turner, D. J., Miretti, M., Rajan, D., Regler, H., Carter, N. P., Blayney, M. L., Beck, S. and Hurles, M.E. (2008) Germline rates of de novo meiotic deletions and duplications causing several genomic disorders. Nat. Genet. 40, 90-95