The frequency of heterologous synapsis increases with aging in Robertsonian heterozygous male mice

Chromosome Research

Volumn 20, Issue 2, 2012, Pages 269-278

  Vasco, Chiara ^a,e   Manterola, Marcia ^b,f   Page, Jesus ^c   Zuccotti, Maurizio ^d   De La Fuente, Roberto ^c   Redi, Carlo Alberto ^a   Fernandez Donoso, Raul ^b   Garagna, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d UNIVERSITY OF PARMA   (Italy)

^e DEPARTMENT OF NEUROSURGERY   (Italy)

^f NewYork Presbyterian Hospital   (United States)

Author keywords

Aging; Asynapsis; Meiosis; MSUC; Robertsonian translocation; Spermatogenesis

Indexed keywords

HISTONE H2AX; HISTONE H2AX GAMMA; UNCLASSIFIED DRUG;

AGING; ARTICLE; CHROMOSOME PAIRING; HETEROZYGOTE; IMMUNOCYTOCHEMISTRY; IMMUNOLOCALIZATION; MALE; MEIOSIS; MEIOTIC SILENCING OF UNSYNAPED CHROMATIN; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; SPERMATOCYTE; SPERMATOGENESIS;

AGING; ANIMALS; CHROMOSOME PAIRING; HETEROZYGOTE; MALE; MICE; SEX CHROMOSOMES; SPERMATOCYTES; TRANSLOCATION, GENETIC;

MUS; MUS MUSCULUS; ROBERTSONIA; SYNAPSIS;

EID: 84863603032     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-011-9272-x     Document Type: Article

References (38)

1. Baarends WM, Wassenaar E, van der Laan R, Hoogerbrugge J, Sleddens-Linkels E, Hoeijmakers JH, de Boer P, Grootegoed JA (2005) Silencing ofunpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 25:1041-1053 (Pubitemid 40165811)
2. Britton-Davidian J, Catalan J, da Graca Ramalhinho M, Ganem G, Auffray JC, Capela R, Biscoito M, Searle JB, da Luz Mathias M (2000) Rapid chromosomal evolution in island mice. Nature 403:158 (Pubitemid 30050950)
3. Burgoyne PS, Mahadevaiah SK, Turner JM (2009) The conse-quences of asynapsis for mammalian meiosis. Nat Rev Genet 10:207-216
4. Capanna E, Redi CA (1995) Whole-arm reciprocal translocation (WART) between Robertsonian chromosomes: finding of a Robertsonian heterozygous mouse with karyotype derived through WARTs. Chromosome Res 3:135-137
5. Capanna E, Gropp A, Winking H, Noack G, Civitelli MV (1976) Robertsonian metacentrics in the mouse. Chromo-soma 58:341-353
6. Eaker S, Pyle A, Cobb J, Handel MA (2001) Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. J Cell Sci 114:2953-2965 (Pubitemid 32821534)
7. Everett CA, Searle JB, Wallace BM (1996) A study ofmeiotic pairing, nondisjunction and germ cell death in laboratory mice carrying Robertsonian translocations. Genet Res 67:239-247 (Pubitemid 26202588)
8. Garagna S, Redi CA, Zuccotti M, Britton-Davidian J, Winking H (1990) Kinetics of oogenesis in mice heterozygous for Robertsonian translocation. Differentiation 42:167-171 (Pubitemid 20104077)
9. Garagna S, Zuccotti M, Thornhill A, Fernandez-Donoso R, Berrios S, Capanna E, Redi CA (2001a) Alteration of nuclear architecture in male germ cells of chromosomally derived subfertile mice. J Cell Sci 114:4429-4434 (Pubitemid 34082863)
10. Garagna S, Zuccotti M, Vecchi ML, Rubini PG, Capanna E, Redi CA (2001b) Human-dominated ecosystems and res-toration ecology: Seveso today. Chemosphere 43:577-585 (Pubitemid 32405506)
11. Gropp A, Winking H, Redi CA, Capanna E, Britton-Davidian J, Noack G (1982) Robertsonian karyotypevariation in wild house mice from Rhaeto-Lombardia. Cytogenet Cell Genet 34:67-77 (Pubitemid 13208248)
12. Hauffe HC, Searle JB (1998) Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics 150:1143-1154 (Pubitemid 28510042)
13. Homolka D, Ivanek R, Capkova J, Jansa P, Forejt J (2007) Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res 17:1431-1437 (Pubitemid 47529427)
14. Johannisson R, Winking H (1994) Synaptonemal complexes of chains and rings in mice heterozygous for multiple Robertsonian translocations. Chromosome Res 2:137-145 (Pubitemid 24110423)
15. Kouznetsova A, Wang H, Bellani M, Camerini-Otero RD, Jessberger R, Hoog C (2009) BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asyn-apsed chromosomes. J Cell Sci 122:2446-2452
16. Lehmann E, Radbruch A (1977) Robertsonian translocations in Mus musculus from Sicily. Experientia 33:1025-1026 (Pubitemid 8161194)
17. Mahadevaiah SK, Bourc His D, de Rooij DG, Bestor TH, Turner JM, Burgoyne PS (2008) Extensive meiotic asyn-apsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromo-some inactivation. J Cell Biol 182:263-276
18. Manterola M, Page J, Vasco C, Berrios S, Parra MT, Viera A, Rufas JS, Zuccotti M, Garagna S, Fernandez-Donoso R (2009) A high incidence of meiotic silencing of unsynapsed chromatin is not associated with substantial pachytene loss in heterozygous male mice carrying multi-ple simple Robertsonian translocations. PLo S Genet 5: e1000625
19. Merico V, Pigozzi MI, Esposito A, Merani MS, Garagna S (2003) Meiotic recombination and spermatogenic impair-ment in Mus musculus domesticus carrying multiple simple Robertsonian translocations. Cytogenet Genome Res 103:321-329 (Pubitemid 38445997)
20. Merico V, de Barboza GD, Vasco C, Ponce R, Rodriguez V Garagna S, de Talamoni NT (2008) A mitochondrial mech-anism is involved in apoptosis of Robertsonian mouse male germ cells. Reproduction 135:797-804 (Pubitemid 351837392)
21. Moses MJ (1980) New cytogenetic studies on mammalian meiosis. Raven, New York
22. Nicklas RB, Ward SC, Gorbsky GJ (1995) Kinetochore chem-istry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J Cell Biol 130:929-939
23. Nicklas RB, Waters JC, Salmon ED, Ward SC (2001) Check-point signals in grasshopper meiosis are sensitive to micro-tubule attachment, but tension is still essential. J Cell Sci 114:4173-4183 (Pubitemid 33138655)
24. Nunes AC, Catalan J, Lopez J, Ramalhinho MD, Mathias MD, Britton-Davidian J (2011) Fertility assessment in hybrids between monobrachially homologous Rb races of the house mouse from the island of Madeira: implications for modes of chromosomal evolution. Heredity 106:348-356
25. Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique forthe spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5:66-68 (Pubitemid 27129985)
26. Pialek J, Albrecht T (2005) Choosing mates: complementary versus compatible genes. Trends Ecol Evol 20:63 (Pubitemid 40118091)
27. Redi C, Capanna E (1988) Robertsonian heterozygotes in the house mouse and the fate oftheir germ cells. Alan R. Liss Inc., New York
28. Rodriguez V, Diaz de Barboza G, Ponce R, Merico V, Garagna S, Tolosa de Talamoni N (2010) Spermatocyte apoptosis, which involves both intrinsic and extrinsic pathways, explains the sterility of Graomys griseoflavus × Graomys centralis male hybrids. Reprod Fertil Dev 22:478-488
29. Saferali A, Berlivet S, Schimenti J, Bartolomei MS, Taketo T, Naumova AK (2010) Defective imprint resetting in carriers of Robertsonian translocation Rb (8.12). Mamm Genome 21:377-387
30. Schoenmakers S, Wassenaar E, van Cappellen WA, Derijck AA, de Boer P, Laven JS, Grootegoed JA, Baarends WM (2008) Increased frequency of asynapsis and associated meiotic silencing of heterologous chromatin in the presence of irradiation-induced extra DNA double strand breaks. Dev Biol 317:270-281
31. Sciurano R, Rahn M, Rey-Valzacchi G, Solari AJ (2007) The asynaptic chromatin in spermatocytes of translocation car-riers contains the histone variant gamma-H2AX and asso-ciates with the XY body. Hum Reprod 22:142-150 (Pubitemid 44942678)
32. Searle J (1993) Chromosomal hybrid zones in eutherian mammals. Oxford University Press, Oxford
33. Shiu PK, Metzenberg RL (2002) Meiotic silencing by unpaired DNA: properties, regulation and suppression. Genetics 161:1483-1495 (Pubitemid 35014750)
34. Shiu PK, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107:905-916 (Pubitemid 34084981)
35. Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS (2005) Silencing of unsy-napsed meiotic chromosomes in the mouse. Nat Genet 37:41-47 (Pubitemid 40070938)
36. Turner JM, Mahadevaiah SK, Ellis PJ, Mitchell MJ, Burgoyne PS (2006) Pachytene asynapsis drives meiotic sex chromo-some inactivation and leads to substantial postmeiotic repression in spermatids. Dev Cell 10:521-529
37. Wallace BM, Searle JB, Everett CA (1992) Male meiosis and gametogenesis in wild house mice (Mus musculus domes-ticus) from a chromosomal hybrid zone; a comparison between "simple" Robertsonian heterozygotes and homo-zygotes. Cytogenet Cell Genet 61:211-220
38. Wallace BM, Searle JB, Everett CA (2002) The effect of multiple simple Robertsonian heterozygosity on chro-mosome pairing and fertility of wild-stock house mice (Mus musculus domesticus). Cytogenet Genome Res 96:276-286 (Pubitemid 37456609)