Chromosome Research

, Volume 10, Issue 7, pp 549–560 | Cite as

Differential association of SMC1α and SMC3 proteins with meiotic chromosomes in wild-type and SPO11-deficient male mice

  • Rosalina D. James
  • John A. Schmiesing
  • Antoine H. F. M. Peters
  • Kyoko Yokomori
  • Christine M. Disteche

Abstract

SMC proteins are components of cohesin complexes that function in chromosome cohesion. We determined that SMC1α and SMC3 localized to wild-type mouse meiotic chromosomes, but with distinct differences in their patterns. Anti-SMC3 coincided with axial elements of the synaptonemal complex, while SMC1α was observed mainly in regions where homologues were synapsed. This pattern was especially visible in pachytene sex vesicles where SMC1α localized only weakly to the asynapsed regions. At diplotene, SMC3, but not SMC1α, remained bound along axial elements of desynapsed chromosomes. SMC1α and SMC3 were also found to localize along meiotic chromosome cores of Spo11 null spermatocytes, in which double-strand break formation required for DNA recombination and homologous pairing were disrupted. In Spo11−/− cells, SMC1α localization differed from SMC3 again, confirming that SMC1α is mainly associated with homologous or non-homologous synapsed regions, whereas SMC3 localized throughout the chromosomes. Our results suggest that the two cohesin proteins may not always be associated in a dimer and may function as separate complexes in mammalian meiosis, with SMC1α playing a more specific role in synapsis. In addition, our results indicate that cohesin cores can form independently of double-strand break formation and homologous pairing.

meiotic chromosomes SMC1α SMC3 SPO11 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ball AR, Yokomori K (2001) The structural maintenance of chromosomes (SMC) family of proteins in mammals. Chromosome Res 9: 85-96.CrossRefGoogle Scholar
  2. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking spo11. Mol Cell 6: 989-998.PubMedCrossRefGoogle Scholar
  3. Cao L, Alani E, Kleckner N (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089-1101.PubMedCrossRefGoogle Scholar
  4. Darwiche N, Freeman LA, Strunnikov A (1999) Characterization of the components of the putative mammalian sister chromatid cohesion complex. Gene 233: 39-47.PubMedCrossRefGoogle Scholar
  5. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107: 2749-2760.PubMedGoogle Scholar
  6. Dresser ME, Giroux CN (1988) Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol 106: 567-573.PubMedCrossRefGoogle Scholar
  7. 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: 673-682.PubMedGoogle Scholar
  8. Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. Embo J 20: 589-600.PubMedCrossRefGoogle Scholar
  9. Guacci V, Koshland D, Strunnikov A (1997) A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91: 47-57.PubMedCrossRefGoogle Scholar
  10. Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9: 773-788.PubMedCrossRefGoogle Scholar
  11. Heyting C, Moens PB, van Raamsdonk W, Dietrich AJ, Vink AC, Redeker EJ (1987) Identification of two major components of the lateral elements of synaptonemal complexes of the rat. Eur J Cell Biol 43: 148-154.PubMedGoogle Scholar
  12. Jessberger R, Riwar B, Baechtold H, Akhmedov AT (1996) SMC proteins constitute two subunits of the mammalian recombination complex RC-1. Embo J 15: 4061-4068.PubMedGoogle Scholar
  13. Keeney S, Baudat F, Angeles M et al. (1999) A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics 61: 170-182.PubMedCrossRefGoogle Scholar
  14. Klein F, Mahr P, Galova M et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91-103.PubMedCrossRefGoogle Scholar
  15. Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14: 1137-1146.PubMedGoogle Scholar
  16. Loidl J, Klein F, Scherthan H (1994) Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J Cell Biol 125: 1191-1200.PubMedCrossRefGoogle Scholar
  17. Losada A, Hirano M, Hirano T (1998) Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12: 1986-1997.PubMedGoogle Scholar
  18. Meuwissen RL, Offenberg HH, Dietrich AJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. Embo J 11: 5091-5100.PubMedGoogle Scholar
  19. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45.PubMedCrossRefGoogle Scholar
  20. Moens PB, Spyropoulos B (1995) Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma 104: 175-182.PubMedGoogle Scholar
  21. Moens PB, Heyting C, Dietrich AJ, van Raamsdonk W, Chen Q (1987) Synaptonemal complex antigen location and conservation. J Cell Biol 105: 93-103.PubMedCrossRefGoogle Scholar
  22. Moens PB, Freire R, Tarsounas M, Spyropoulos B, Jackson SP (2000) Expression and nuclear localization of BLM, a chromosome stability protein mutated in Bloom's syndrome, suggest a role in recombination during meiotic prophase. JCell Sci 113: 663-672.Google Scholar
  23. Pelttari J, Hoja MR, Yuan L 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.PubMedCrossRefGoogle Scholar
  24. Pezzi N, Prieto I, Kremer L et al. (2000) STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 14: 581-592.PubMedGoogle Scholar
  25. Prieto I, Suja JA, Pezzi N et al. (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3: 761-766.PubMedCrossRefGoogle Scholar
  26. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21: 6984-6998.PubMedCrossRefGoogle Scholar
  27. Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11: 2600-2621.PubMedGoogle Scholar
  28. Romanienko PJ, Camerini-Otero RD (2000) The mouse spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6: 975-987.PubMedCrossRefGoogle Scholar
  29. Schmiesing JA, Ball AR Jr., Gregson HC, Alderton JM, Zhou S, Yokomori K (1998) Identification of two distinct human SMC protein complexes involved in mitotic chromosome dynamics. Proc Natl Acad Sci USA 95: 12906-12911.PubMedCrossRefGoogle Scholar
  30. Strunnikov AV, Jessberger R (1999) Structural maintenance of chromosomes (SMC) proteins: conserved molecular properties for multiple biological functions. Eur J Biochem, 263: 6-13.PubMedCrossRefGoogle Scholar
  31. Sumara I, Vorlaufer E, Gieffers C, Peters BH, Peters JM (2000) Characterization of vertebrate cohesin complexes and their regulation in prophase. J Cell Biol 151: 749-762.PubMedCrossRefGoogle Scholar
  32. Uhlmann F, Nasmyth K (1998) Cohesion between sister chromatids must be established during DNA replication. Curr Biol 8: 1095-1101.PubMedCrossRefGoogle Scholar
  33. Van Heemst D, Heyting C (2000) Sister chromatid cohesion and recombination in meiosis. Chromosoma 109: 10-26.PubMedCrossRefGoogle Scholar
  34. Weiner BM, Kleckner N (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77: 977-991.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Rosalina D. James
    • 1
  • John A. Schmiesing
    • 2
  • Antoine H. F. M. Peters
    • 3
    • 4
  • Kyoko Yokomori
    • 2
  • Christine M. Disteche
    • 1
  1. 1.Department of PathologyUniversity of WashingtonSeattle
  2. 2.Department of Biological ChemistryUniversity of CaliforniaIrvineUSA
  3. 3.Department of GeneticsUniversity of WashingtonSeattle
  4. 4.Research Institute of Molecular PathologyViennaAustria

Personalised recommendations