Chromosoma

, Volume 115, Issue 3, pp 235–240 | Cite as

Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins

Mini-Review

Abstract

Recent progress in elucidating the function of synaptonemal complex (SC) proteins and of cohesins in meiocytes made possible, in particular, through the analysis of mice deficient in SC or cohesin proteins has significantly enriched our understanding of how meiotic chromosome architecture is determined. Cohesins and the SC proteins act together in generating the characteristic axis-loop structure of meiotic chromosomes, their pairing into bivalents, their ability to recombine, and to be properly segregated. This minireview attempts to summarize the current knowledge with a focus on higher eukaryotic systems and to ask questions that ought to be addressed in the future.

References

  1. Anderson LK, Royer SM, Page SL, McKim KS, Lai A, Lilly MA, Hawley RS (2005) Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc Natl Acad Sci U S A 102:4482–4487PubMedCrossRefGoogle Scholar
  2. Bannister LA, Reinholdt LG, Munroe RJ, Schimenti JC (2004) Positional cloning and characterization of mouse mei8, a disrupted allele of the meiotic cohesin Rec8. Genesis 40:184–194PubMedCrossRefGoogle Scholar
  3. Chuma S, Nakatsuji N (2001) Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev Biol 229:468–479PubMedCrossRefGoogle Scholar
  4. de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376–1389PubMedCrossRefGoogle Scholar
  5. 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):673–682PubMedGoogle Scholar
  6. Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J Cell Biol 160:657–670PubMedCrossRefGoogle Scholar
  7. Firooznia A, Revenkova E, Jessberger R (2005) From the XXVII North American testis workshop: the function of SMC and other cohesin proteins in meiosis. J Androl 26:1–10PubMedGoogle Scholar
  8. Hagstrom KA, Meyer BJ (2003) Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4:520–534PubMedCrossRefGoogle Scholar
  9. Heidmann D, Horn S, Heidmann S, Schleiffer A, Nasmyth K, Lehner CF (2004) The Drosophila meiotic kleisin C(2)M functions before the meiotic divisions. Chromosoma 113:177–187PubMedCrossRefGoogle Scholar
  10. Hirano T (2005) SMC proteins and chromosome mechanics: from bacteria to humans. Philos Trans R Soc Lond B Biol Sci 360:507–514PubMedCrossRefGoogle Scholar
  11. 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 37:1351–1355PubMedCrossRefGoogle Scholar
  12. Jessberger R (2002) The many functions of SMC proteins in chromosome dynamics. Nat Rev Mol Cell Biol 3:767–778PubMedCrossRefGoogle Scholar
  13. Kim JS, Krasieva TB, LaMorte V, Taylor AM, Yokomori K (2002) Specific recruitment of human cohesin to laser-induced DNA damage. J Biol Chem 277:45149–45153PubMedCrossRefGoogle Scholar
  14. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98:91–103PubMedCrossRefGoogle Scholar
  15. Kolas NK, Yuan L, Hoog C, Heng HH, Marcon E, Moens PB (2004) Male mouse meiotic chromosome cores deficient in structural proteins SYCP3 and SYCP2 align by homology but fail to synapse and have possible impaired specificity of chromatin loop attachment. Cytogenet Genome Res 105:182–188PubMedCrossRefGoogle Scholar
  16. Kouznetsova A, Novak I, Jessberger R, Hoog C (2005) SYCP2 and SYCP3 are required for cohesin core integrity at diplotene but not for centromere cohesion at the first meiotic division. J Cell Sci 118:2271–2278PubMedCrossRefGoogle Scholar
  17. Liebe B, Alsheimer M, Hoog C, Benavente R, Scherthan H (2004) Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements. Mol Biol Cell 15:827–837PubMedCrossRefGoogle Scholar
  18. Manheim EA, McKim KS (2003) The synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila. Curr Biol 13:276–285PubMedCrossRefGoogle Scholar
  19. 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 117:1221–1234PubMedCrossRefGoogle Scholar
  20. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J (2001) A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev 15:1349–1360PubMedCrossRefGoogle Scholar
  21. Pelttari J, Hoja MR, Yuan L, Liu JG, Brundell E, Moens P, Santucci-Darmanin S, Jessberger R, Barbero JL, Heyting C, Hoog 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 21:5667–5677PubMedCrossRefGoogle Scholar
  22. Prieto I, Suja JA, Pezzi N, Kremer L, Martinez AC, Rufas JS, Barbero JL (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3:761–766PubMedCrossRefGoogle Scholar
  23. Prieto I, Pezzi N, Buesa JM, Kremer L, Barthelemy I, Carreiro C, Roncal F, Martinez A, Gomez L, Fernandez R, Martinez AC, Barbero JL (2002) STAG2 and Rad21 mammalian mitotic cohesins are implicated in meiosis. EMBO Rep 3:543–550PubMedCrossRefGoogle Scholar
  24. Revenkova E, Jessberger R (2005) Keeping sister chromatids together: cohesins in meiosis. Reproduction 130:783–790PubMedCrossRefGoogle Scholar
  25. Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21:6984–6998PubMedCrossRefGoogle Scholar
  26. Revenkova E, Eijpe M, Heyting C, Hodges CA, Hunt PA, Liebe B, Scherthan H, Jessberger R (2004) Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat Cell Biol 6:555–562PubMedCrossRefGoogle Scholar
  27. Strom L, Sjogren C (2005) DNA damage-induced cohesion. Cell Cycle 4:536–539PubMedGoogle Scholar
  28. Strom L, Lindroos HB, Shirahige K, Sjogren C (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16:1003–1015PubMedCrossRefGoogle Scholar
  29. Trelles-Sticken E, Adelfalk C, Loidl J, Scherthan H (2005) Meiotic telomere clustering requires actin for its formation and cohesin for its resolution. J Cell Biol 170:213–223PubMedCrossRefGoogle Scholar
  30. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16:991–1002PubMedCrossRefGoogle Scholar
  31. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464PubMedCrossRefGoogle Scholar
  32. Xu H, Beasley M, Verschoor S, Inselman A, Handel MA, McKay MJ (2004) A new role for the mitotic RAD21/SCC1 cohesin in meiotic chromosome cohesion and segregation in the mouse. EMBO Rep 5:378–384PubMedCrossRefGoogle Scholar
  33. Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8:949–961PubMedCrossRefGoogle Scholar
  34. Yuan L, Liu JG, Hoja MR, Wilbertz J, Nordqvist K, Hoog C (2002) Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 296:1115–1118PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Department of Gene and Cell MedicineMount Sinai School of MedicineNew York,USA
  2. 2.Institute of Physiological ChemistryDresden University of TechnologyDresdenGermany

Personalised recommendations