Cohesin axis maturation and presence of RAD51 during first meiotic prophase in a true bug

Chromosoma

Volumn 118, Issue 5, 2009, Pages 575-589

  Viera, Alberto ^a   Santos, Juan Luis ^b   Parra, María Teresa ^a   Calvente, Adela ^a   Gómez, Rocío ^a   Fuente, Roberto ^a   Suja, José Ángel ^a   Page, Jesús ^a   Rufas, Julio S ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; COHESIN; HISTONE H3; LYSINE; PROTEIN SMC1 ALPHA; PROTEIN SMC3; RAD51 PROTEIN; STRUCTURAL MAINTENANCE CHROMOSOME 1 ALPHA PROTEIN; STRUCTURAL MAINTENANCE CHROMOSOME 3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHROMOSOMAL LOCALIZATION; CHROMOSOME PAIRING; CHROMOSOME STRUCTURE; DEVELOPMENTAL STAGE; ENZYME LOCALIZATION; GRAPHOSOMA ITALICUM; HEMIPTERA; HETEROCHROMATIN; MALE; MEIOSIS; MITOTIC RECOMBINATION; NONHUMAN; PACHYTENE; PROPHASE; PROTEIN LOCALIZATION; SPERMATOCYTE; SYNAPTONEMAL COMPLEX; X CHROMOSOME; Y CHROMOSOME;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES; HEMIPTERA; HISTONES; MALE; MEIOTIC PROPHASE I; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SPERMATOCYTES; SYNAPTONEMAL COMPLEX;

GRAPHOSOMA; HEMIPTERA; HETEROPTERA; PENTATOMIDAE; SYNAPSIS;

EID: 69249222719     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-009-0218-4     Document Type: Article

References (48)

1. Calvente A, Viera A, Page J, Parra MT, Gomez R, Suja JA, Rufas JS, Santos JL (2005) DNA double-strand breaks and homology search: inferences from a species with incomplete pairing and synapsis. J Cell Sci 118:2957-2963
2. Cardoso H, Stoll M, Dutra A, Oliver G, Di Tomaso MV (1986) Characterization of the diffuse stage in the male meiotic prophase and karyotype of Scapteriscus borellii (Orthoptera: Grylloidea). Genetica 71:23-29
3. Darlington CD, LaCour LF (1969) The handling of chromosomes. Allen and Unwin, London
4. de la Fuente R, Parra MT, Viera A, Calvente A, Gomez R, Suja JA, Rufas JS, Page J (2007) Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: The role of SYCP3 protein. PLoS Genet 3:e198
5. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387-398
6. Eijpe M, Heyting C, Gross B, Jessberger R (2000) Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes. J Cell Sci 113(Pt 4):673-682
7. Esponda P, Stockert JC (1978) Localization of the synaptonemal complex under the light microscope. Chromosoma 68:83-90
8. Garcia M, Dietrich AJ, Freixa L, Vink AC, Ponsa M, Egozcue J (1987) Development of the first meiotic prophase stages in human fetal oocytes observed by light and electron microscopy. Hum Genet 77:223-232
9. Garcia-Cao M, O'Sullivan R, Peters AH, Jenuwein T, Blasco MA (2004) Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36:94-99
10. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20:589-600
11. Henderson KA, Keeney S (2005) Synaptonemal complex formation: Where does it start? Bioessays 27:995-998
12. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA (2005) SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37:1351-1355
13. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074-1080
14. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300:1152-1155
15. Klásterská I (1976) A new look on the role of the diffuse stage in problems of plant and animal species. Hereditas 82:193-204
16. Klásterská I (1977) The concept of the prophase on meiosis. Hereditas 86:205-210
17. Kleckner N (1996) Meiosis: How could it work? Proc Natl Acad Sci U S A 93:8167-8174
18. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271-276
19. McKim KS, 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
20. Nicklas RB, Kubai DF, Hays TS (1982) Spindle microtubules and their mechanical associations after micromanipulation in anaphase. J Cell Biol 95:91-104
21. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20:525-558
22. Page J, Suja JA, Santos JL, Rufas JS (1998) Squash procedure for protein immunolocalization in meiotic cells. Chromosome Res 6:639-642
23. Page J, Berrios S, Rufas JS, Parra MT, Suja JA, Heyting C, Fernandez-Donoso R (2003) The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements. J Cell Sci 116:551-560
24. Page J, de la Fuente R, Gomez R, Calvente A, Viera A, Parra MT, Santos JL, Berrios S, Fernandez-Donoso R, Suja JA et al (2006) Sex chromosomes, synapsis, and cohesins: A complex affair. Chromosoma 115:250-259
25. Parra MT, Page J, Yen TJ, He D, Valdeolmillos A, Rufas JS, Suja JA (2002) Expression and behaviour of CENP-E at kinetochores during mouse spermatogenesis. Chromosoma 111:53-61
26. Parra MT, Viera A, Gomez R, Page J, Benavente R, Santos JL, Rufas JS, Suja JA (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117:1221-1234
27. Pelttari J, Hoja MR, Yuan L, Liu JG, Brundell E, Moens P, Santucci-Darmanin S, Jessberger R, Barbero JL, Heyting C et al (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
28. Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germ line. Chromosome Res 5:66-68
29. Peters AH, O'Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A et al (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323-337
30. Pigozzi MI, Solari AJ (2003) Differential immunolocalization of a putative Rec8p in meiotic autosomes and sex chromosomes of triatomine bugs. Chromosoma 112:38-47
31. Prieto I, Tease C, Pezzi N, Buesa JM, Ortega S, Kremer L, Martinez A, Martinez AC, Hulten MA, Barbero JL (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res 12:197-213
32. Revenkova E, Jessberger R (2005) Keeping sister chromatids together: cohesins in meiosis. Reproduction 130:783-790
33. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21:6984-6998
34. Roeder GS (1997) Meiotic chromosomes: It takes two to tango. Genes Dev 11:2600-2621
35. Rufas JS, Gimenez-Martin G (1986) Ultrastructure of the kinetochore in Graphosoma italicum (Hemiptera, Heteroptera). Protoplasma 132:142-148
36. Stockert JC (1977) Osmium tetroxide/p-phenylenediamine staining of nucleoli and Balbiani rings in Chironomus salivary glands. Histochemistry 53:43-56
37. Storlazzi A, Tesse S, Ruprich-Robert G, Gargano S, Poggeler S, Kleckner N, Zickler D (2008) Coupling meiotic chromosome axis integrity to recombination. Genes Dev 22:796-809
38. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45
39. Suja JA, del Cerro AL, Page J, Rufas JS, Santos JL (2000) Meiotic sister chromatid cohesion in holocentric sex chromosomes of three heteropteran species is maintained in absence of axial elements. Chromosoma 109:35-43
40. Tesse S, Storlazzi A, Kleckner N, Gargano S, Zickler D (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A 100:12865-12870
41. Valdeolmillos AM, Viera A, Page J, Prieto I, Santos JL, Parra MT, Heck MM, Martinez AC, Barbero JL, Suja JA et al (2007) Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers. PLoS Genet 3:e28
42. Viera A, Parra MT, Page J, Santos JL, Rufas JS, Suja JA (2003) Dynamic relocation of telomere complexes in mouse meiotic chromosomes. Chromosome Res 11:797-807
43. Viera A, Calvente A, Page J, Parra MT, Gomez R, Suja JA, Rufas JS, Santos JL (2004a) X and B chromosomes display similar meiotic characteristics in male grasshoppers. Cytogenet Genome Res 106:302-308
44. Viera A, Santos JL, Page J, Parra MT, Calvente A, Cifuentes M, Gomez R, Lira R, Suja JA, Rufas JS (2004b) DNA double-strand breaks, recombination and synapsis: The timing of meiosis differs in grasshoppers and flies. EMBO Rep 5:385-391
45. Viera A, Page J, Rufas JS (2009a) Inverted meiosis: The true bugs as a model to study. Genome Dyn 5:137-156
46. Viera A, Santos JL, Rufas JS (2009b) Relationship between incomplete synapsis and chiasma localization. Chromosoma 118:377-389
47. Wilson EB (1928) The cell in development and heredity. Macmillan, New York
48. Zickler D, Kleckner N (1999) Meiotic chromosomes: Integrating structure and function. Annu Rev Genet 33:603-754