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. 2002 Nov;162(3):1367–1379. doi: 10.1093/genetics/162.3.1367

Sex-specific differences in meiotic chromosome segregation revealed by dicentric bridge resolution in mice.

Kara E Koehler 1, Elise A Millie 1, Jonathan P Cherry 1, Paul S Burgoyne 1, Edward P Evans 1, Patricia A Hunt 1, Terry J Hassold 1
PMCID: PMC1462335  PMID: 12454080

Abstract

The meiotic properties of paracentric inversion heterozygotes have been well studied in insects and plants, but not in mammalian species. In essence, a single meiotic recombination event within the inverted region results in the formation of a dicentric chromatid, which usually breaks or is stretched between the two daughter nuclei during the first meiotic anaphase. Here, we provide evidence that this is not the predominant mode of exchange resolution in female mice. In sharp contrast to previous observations in other organisms, we find that attempts to segregate the dicentric chromatid frequently result not in breakage, stretching, or loss, but instead in precocious separation of the sister centromeres of at least one homolog. This often further results in intact segregation of the dicentric into one of the meiotic products, where it can persist into the first few embryonic divisions. These novel observations point to an unusual mechanism for the processing of dicentric chromosomes in mammalian oogenesis. Furthermore, this mechanism is rare or nonexistent in mammalian spermatogenesis. Thus, our results provide additional evidence of sexual dimorphism in mammalian meiotic chromosome behavior; in "stressful" situations, meiotic sister chromatid cohesion is apparently handled differently in males than in females.

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Selected References

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  1. Bean C. J., Hunt P. A., Millie E. A., Hassold T. J. Analysis of a malsegregating mouse Y chromosome: evidence that the earliest cleavage divisions of the mammalian embryo are non-disjunction-prone. Hum Mol Genet. 2001 Apr 15;10(9):963–972. doi: 10.1093/hmg/10.9.963. [DOI] [PubMed] [Google Scholar]
  2. Borodin P. M., Gorlov I. P., Ladygina TYu Synapsis in single and double heterozygotes for partially overlapping inversions in chromosome 1 of the house mouse. Chromosoma. 1990 Sep;99(5):365–370. doi: 10.1007/BF01731725. [DOI] [PubMed] [Google Scholar]
  3. Borodin P. M., Gorlov I. P., Ladygina TYu Synaptic interrelationships between the segments of the heteromorphic bivalent in double heterozygotes for paracentric inversions in chromosome 1 of the house mouse. Chromosoma. 1992 Mar;101(5-6):374–379. doi: 10.1007/BF00346017. [DOI] [PubMed] [Google Scholar]
  4. Burgoyne P. S. A Y-chromosomal effect on blastocyst cell number in mice. Development. 1993 Jan;117(1):341–345. doi: 10.1242/dev.117.1.341. [DOI] [PubMed] [Google Scholar]
  5. Burgoyne P. S., Evans E. P. A high frequency of XO offspring from X(Paf)Y* male mice: evidence that the Paf mutation involves an inversion spanning the X PAR boundary. Cytogenet Cell Genet. 2000;91(1-4):57–61. doi: 10.1159/000056819. [DOI] [PubMed] [Google Scholar]
  6. Carson D. R., Christman M. F. Evidence that replication fork components catalyze establishment of cohesion between sister chromatids. Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8270–8275. doi: 10.1073/pnas.131022798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chandley A. C. A pachytene analysis of two male-fertile paracentric inversions in chromosome 1 of the mouse and in the male-sterile double heterozygote. Chromosoma. 1982;85(1):127–135. doi: 10.1007/BF00344599. [DOI] [PubMed] [Google Scholar]
  8. EVANS E. P., BRECKON G., FORD C. E. AN AIR-DRYING METHOD FOR MEIOTIC PREPARATIONS FROM MAMMALIAN TESTES. Cytogenetics. 1964;3:289–294. doi: 10.1159/000129818. [DOI] [PubMed] [Google Scholar]
  9. Evans E. P., Phillips R. J. Inversion heterozygosity and the origin of XO daughters of Bpa/+female mice. Nature. 1975 Jul 3;256(5512):40–41. doi: 10.1038/256040a0. [DOI] [PubMed] [Google Scholar]
  10. Gorlov I. P., Borodin P. M. Recombination in single and double heterozygotes for two partially overlapping inversions in chromosome 1 of the house mouse. Heredity (Edinb) 1995 Aug;75(Pt 2):113–125. doi: 10.1038/hdy.1995.114. [DOI] [PubMed] [Google Scholar]
  11. Haber J. E., Thorburn P. C., Rogers D. Meiotic and mitotic behavior of dicentric chromosomes in Saccharomyces cerevisiae. Genetics. 1984 Feb;106(2):185–205. doi: 10.1093/genetics/106.2.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hodges C. A., LeMaire-Adkins R., Hunt P. A. Coordinating the segregation of sister chromatids during the first meiotic division: evidence for sexual dimorphism. J Cell Sci. 2001 Jul;114(Pt 13):2417–2426. doi: 10.1242/jcs.114.13.2417. [DOI] [PubMed] [Google Scholar]
  13. Hunt P., LeMaire R., Embury P., Sheean L., Mroz K. Analysis of chromosome behavior in intact mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum Mol Genet. 1995 Nov;4(11):2007–2012. doi: 10.1093/hmg/4.11.2007. [DOI] [PubMed] [Google Scholar]
  14. Hunt Patricia A., Hassold Terry J. Sex matters in meiosis. Science. 2002 Jun 21;296(5576):2181–2183. doi: 10.1126/science.1071907. [DOI] [PubMed] [Google Scholar]
  15. LeMaire-Adkins R., Hunt P. A. Nonrandom segregation of the mouse univalent X chromosome: evidence of spindle-mediated meiotic drive. Genetics. 2000 Oct;156(2):775–783. doi: 10.1093/genetics/156.2.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moses M. J., Poorman P. A., Roderick T. H., Davisson M. T. Synaptonemal complex analysis of mouse chromosomal rearrangements. IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma. 1982;84(4):457–474. doi: 10.1007/BF00292848. [DOI] [PubMed] [Google Scholar]
  17. Pardo-Manuel de Villena F., Sapienza C. Female meiosis drives karyotypic evolution in mammals. Genetics. 2001 Nov;159(3):1179–1189. doi: 10.1093/genetics/159.3.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Roderick T. H., Hawes N. L. Nineteen paracentric chromosomal inversions in mice. Genetics. 1974 Jan;76(1):109–117. doi: 10.1093/genetics/76.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Roderick T. H. Producing and detecting paracentric chromosomal inversions in mice. Mutat Res. 1971 Jan;11(1):59–69. doi: 10.1016/0027-5107(71)90032-7. [DOI] [PubMed] [Google Scholar]
  20. Rumpler Y., Gabriel-Robez O., Volobouev V., Yu W., Rasamimanana P., de Perdigo A. Male sterility and double heterozygosity for chromosomal inversion. Cytogenet Cell Genet. 1995;69(1-2):66–70. doi: 10.1159/000133940. [DOI] [PubMed] [Google Scholar]
  21. Sturtevant A H, Beadle G W. The Relations of Inversions in the X Chromosome of Drosophila Melanogaster to Crossing over and Disjunction. Genetics. 1936 Sep;21(5):554–604. doi: 10.1093/genetics/21.5.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tease C., Fisher G. Further examination of the production-line hypothesis in mouse foetal oocytes. I. Inversion heterozygotes. Chromosoma. 1986;93(5):447–452. doi: 10.1007/BF00285827. [DOI] [PubMed] [Google Scholar]
  23. Wang Z., Castaño I. B., De Las Peñas A., Adams C., Christman M. F. Pol kappa: A DNA polymerase required for sister chromatid cohesion. Science. 2000 Aug 4;289(5480):774–779. doi: 10.1126/science.289.5480.774. [DOI] [PubMed] [Google Scholar]
  24. Worsham M. J., Miller D. A., Devries J. M., Mitchell A. R., Babu V. R., Surli V., Weiss L., Van Dyke D. L. A dicentric recombinant 9 derived from a paracentric inversion: phenotype, cytogenetics, and molecular analysis of centromeres. Am J Hum Genet. 1989 Jan;44(1):115–123. [PMC free article] [PubMed] [Google Scholar]

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