, Volume 122, Issue 1–2, pp 77–91 | Cite as

Dynamics of cohesin subunits in grasshopper meiotic divisions

  • A. Calvente
  • A. Viera
  • M. T. Parra
  • R. de la Fuente
  • J. A. Suja
  • J. Page
  • J. L. Santos
  • C. García de la Vega
  • J. L. Barbero
  • J. S. RufasEmail author
Research Article


The cohesin complex plays a key role for the maintenance of sister chromatid cohesion and faithful chromosome segregation in both mitosis and meiosis. This complex is formed by two structural maintenance of chromosomes protein family (SMC) subunits and two non-SMC subunits: an α-kleisin subunit SCC1/RAD21/REC8 and an SCC3-like protein. Several studies carried out in different species have revealed that the distribution of the cohesin subunits along the chromosomes during meiotic prophase I is not regular and that some subunits are distinctly incorporated at different cell stages. However, the accurate distribution of the different cohesin subunits in condensed meiotic chromosomes is still controversial. Here, we describe the dynamics of the cohesin subunits SMC1α, SMC3, RAD21 and SA1 during both meiotic divisions in grasshoppers. Although these subunits show a similar patched labelling at the interchromatid domain of metaphase I bivalents, SMCs and non-SMCs subunits do not always colocalise. Indeed, SA1 is the only cohesin subunit accumulated at the centromeric region of all metaphase I chromosomes. Additionally, non-SMC subunits do not appear at the interchromatid domain in either single X or B chromosomes. These data suggest the existence of several cohesin complexes during metaphase I. The cohesin subunits analysed are released from chromosomes at the beginning of anaphase I, with the exception of SA1 which can be detected at the centromeres until telophase II. These observations indicate that the cohesin components may be differentially loaded and released from meiotic chromosomes during the first and second meiotic divisions. The roles of these cohesin complexes for the maintenance of chromosome structure and their involvement in homologous segregation at first meiotic division are proposed and discussed.


Sister Chromatid Meiotic Division Meiotic Prophase Sister Chromatid Cohesion Supplemental Movie 
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This work was supported by grants BFU2009-10987 and BFU2009-08975 from Ministerio de Ciencia e Innovación (Spain), and grant SAF2011-28842 from Ministerio de Economía y Competitividad (Spain). Adela Calvente had a pre-doctoral contract in Universidad Autónoma de Madrid financed by Consejería de Educación de la Comunidad de Madrid and Fondo Social Europeo during the development of the research. We would like to express our sincere gratitude to the anonymous reviewers for their suggestions.

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  1. Adelfalk C, Janschek J, Revenkova E, Blei C, Liebe B, Gob E, Alsheimer M, Benavente R, de Boer E, Novak I, Hoog C, Scherthan H, Jessberger R (2009) Cohesin SMC1beta protects telomeres in meiocytes. J Cell Biol 187:185–199PubMedCrossRefGoogle Scholar
  2. Barbero JL (2009) Cohesins: chromatin architects in chromosome segregation, control of gene expression and much more. Cell and Mol Life Sci: CMLS 66:2025–2035CrossRefGoogle Scholar
  3. Camacho JP, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philosophical transactions of the Royal Society of London Series B Biol Sci 355:163–178CrossRefGoogle Scholar
  4. Canudas S, Smith S (2009) Differential regulation of telomere and centromere cohesion by the Scc3 homologues SA1 and SA2, respectively, in human cells. J Cell Biol 187:165–173PubMedCrossRefGoogle Scholar
  5. Cobbe N, Heck MM (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol Biol Evol 21:332–347PubMedCrossRefGoogle Scholar
  6. Darlington CD, LaCour LF (1969) The handling of chromosomes. Allen & Unwin, London, 272 ppGoogle Scholar
  7. Dorsett D (2011) Cohesin: genomic insights into controlling gene transcription and development. Curr Opin Genet Dev 21:199–206PubMedCrossRefGoogle Scholar
  8. Dorsett D, Eissenberg JC, Misulovin Z, Martens A, Redding B, McKim K (2005) Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. Development 132:4743–4753PubMedCrossRefGoogle Scholar
  9. Gause M, Webber HA, Misulovin Z, Haller G, Rollins RA, Eissenberg JC, Bickel SE, Dorsett D (2008) Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117:51–66PubMedCrossRefGoogle Scholar
  10. 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 91:47–57PubMedCrossRefGoogle Scholar
  11. Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Suja JA, Barbero JL, Llano E, Pendas AM (2011) Identification and molecular characterization of the mammalian alpha-kleisin RAD21L. Cell Cycle 10:1477–1487PubMedCrossRefGoogle Scholar
  12. Haering CH, Lowe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788PubMedCrossRefGoogle Scholar
  13. Henriques-Gil N, Santos JL, Giraldez R (1982) B-chromosome polymorphism and interchromosomal chiasma interference in Eyprepocnemis plorans (Acrididae; Orthoptera). Chromosoma 85:349–359CrossRefGoogle Scholar
  14. Horsfield JA, Anagnostou SH, Hu JK, Cho KH, Geisler R, Lieschke G, Crosier KE, Crosier PS (2007) Cohesin-dependent regulation of Runx genes. Development 134:2639–2649PubMedCrossRefGoogle Scholar
  15. Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO reports 12:267–275PubMedCrossRefGoogle Scholar
  16. Khetani RS, Bickel SE (2007) Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J Cell Sci 120:3123–3137PubMedCrossRefGoogle Scholar
  17. King M, John B (1980) Regularities and restrictions governing C-band variation in acridoid grasshoppers. Chromosoma 76:123–150CrossRefGoogle Scholar
  18. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y (2003) Distinct cohesin complexes organize meiotic chromosome domains. Science 300:1152–1155PubMedCrossRefGoogle Scholar
  19. Krasikova A, Barbero JL, Gaginskaya E (2005) Cohesion proteins are present in centromere protein bodies associated with avian lampbrush chromosomes. Chromosome Res 13:675–685PubMedCrossRefGoogle Scholar
  20. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  21. Lee J, Hirano T (2011) RAD21L, a novel cohesin subunit implicated in linking homologous chromosomes in mammalian meiosis. J Cell Biol 192:263–276PubMedCrossRefGoogle Scholar
  22. Michaelis C, Ciosk R, Nasmyth K (1997) Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35–45PubMedCrossRefGoogle Scholar
  23. Nasmyth K (2002) Segregating sister genomes: the molecular biology of chromosome separation. Science 297:559–565PubMedCrossRefGoogle Scholar
  24. Nasmyth K (2011) Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 13:1170–1177PubMedCrossRefGoogle Scholar
  25. Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74:595–648PubMedCrossRefGoogle Scholar
  26. Page J, Suja JA, Santos JL, Rufas JS (1998) Squash procedure for protein immunolocalization in meiotic cells. Chromosome Res 6:639–642PubMedCrossRefGoogle Scholar
  27. 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 111:53–61PubMedCrossRefGoogle Scholar
  28. 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
  29. 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 germline. Chromosome Res 5:66–68PubMedCrossRefGoogle Scholar
  30. Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440PubMedCrossRefGoogle Scholar
  31. Pezzi N, Prieto I, Kremer L, Perez Jurado LA, Valero C, Del Mazo J, Martinez AC, Barbero JL (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: Official Publ of the Federation of Am Societies for Exp Biol 14:581–592Google Scholar
  32. 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 reports 3:543–550PubMedCrossRefGoogle Scholar
  33. 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
  34. 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 12:197–213PubMedCrossRefGoogle Scholar
  35. 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
  36. 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
  37. Revenkova E, Jessberger R (2005) Keeping sister chromatids together: cohesins in meiosis. Reproduction 130:783–790PubMedCrossRefGoogle Scholar
  38. Rufas JS, Mazzella C, Garcia de la Vega C, Suja JA (1994) Ultrastructural detection of kinetochores by silver impregnation. Chromosome Res 2:369–375PubMedCrossRefGoogle Scholar
  39. Santos JL, Giraldez R (1978) The effect of C-heterochromatin in chiasma terminalisation in Chorthippus biguttulus L. (Acrididae, Orthoptera). Chromosoma 70:59–66CrossRefGoogle Scholar
  40. Shintomi K, Hirano T (2007) How are cohesin rings opened and closed? Trends Biochem Sci 32:154–157PubMedCrossRefGoogle Scholar
  41. Skibbens RV, Corson LB, Koshland D, Hieter P (1999) Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev 13:307–319PubMedCrossRefGoogle Scholar
  42. Strom L, Lindroos HB, Shirahige K, Sjogren C (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Molecular Cell 16:1003–1015PubMedCrossRefGoogle Scholar
  43. Suja JA, Antonio C, Debec A, Rufas JS (1999) Phosphorylated proteins are involved in sister-chromatid arm cohesion during meiosis I. J Cell Sci 112(Pt 17):2957–2969PubMedGoogle Scholar
  44. Suja JA, Antonio C, Rufas JS (1992) Involvement of chromatid cohesiveness at the centromere and chromosome arms in meiotic chromosome segregation: a cytological approach. Chromosoma 101:493–501PubMedCrossRefGoogle Scholar
  45. Suja JA, Barbero JL (2009) Cohesin complexes and sister chromatid cohesion in mammalian meiosis. Genome Dyn 5:94–116PubMedCrossRefGoogle Scholar
  46. Suja JA, de la Torre J, Gimenez-Abian JF, de la Vega G, Rufas JS (1991) Meiotic chromosome structure. Kinetochores and chromatid cores in standard and B chromosomes of Arcyptera fusca (Orthoptera) revealed by silver staining. Genome 34:19–27PubMedCrossRefGoogle Scholar
  47. Suja JA, Rufas JS (1994) The telochore: a telomeric differentiation of the chromosome axis. Chromosome Res 2:361–368PubMedCrossRefGoogle Scholar
  48. Taagepera S, Rao PN, Drake FH, Gorbsky GJ (1993) DNA topoisomerase II alpha is the major chromosome protein recognized by the mitotic phosphoprotein antibody MPM-2. Proc Natl Acad Sci USA 90:8407–8411PubMedCrossRefGoogle Scholar
  49. Tanaka T, Fuchs J, Loidl J, Nasmyth K (2000) Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation. Nat Cell Biol 2:492–499PubMedCrossRefGoogle Scholar
  50. 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. Molecular Cell 16:991–1002PubMedCrossRefGoogle Scholar
  51. Valdeolmillos AM, Viera A, Page J, Prieto I, Santos JL, Parra MT, Heck MM, Martinez AC, Barbero JL, Suja JA, Rufas JS (2007) Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers. PLoS Genet 3:e28PubMedCrossRefGoogle Scholar
  52. 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 106:302–308PubMedCrossRefGoogle Scholar
  53. Viera A, Gomez R, Parra MT, Schmiesing JA, Yokomori K, Rufas JS, Suja JA (2007) Condensin I reveals new insights on mouse meiotic chromosome structure and dynamics. PLoS One 2:e783PubMedCrossRefGoogle Scholar
  54. 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 reports 5:385–391PubMedCrossRefGoogle Scholar
  55. Viera A, Santos JL, Parra MT, Calvente A, Gomez R, de la Fuente R, Suja JA, Page J, de la Vega CG, Rufas JS (2010) Incomplete synapsis and chiasma localization: the chicken or the egg? Cytogenet Genome Res 128:139–151PubMedCrossRefGoogle Scholar
  56. Viera A, Santos JL, Parra MT, Calvente A, Gomez R, de la Fuente R, Suja JA, Page J, Rufas JS (2009a) Cohesin axis maturation and presence of RAD51 during first meiotic prophase in a true bug. Chromosoma 118:575–589PubMedCrossRefGoogle Scholar
  57. Viera A, Santos JL, Rufas JS (2009b) Relationship between incomplete synapsis and chiasma localization. Chromosoma 118:377–389Google Scholar
  58. Viera A, Santos JL, Rufas JS (2009c) Relationship between incomplete synapsis and chiasma localization. Chromosoma 118:377–389PubMedCrossRefGoogle Scholar
  59. Waizenegger IC, Hauf S, Meinke A, Peters JM (2000) Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103:399–410PubMedCrossRefGoogle Scholar
  60. Warren WD, Steffensen S, Lin E, Coelho P, Loupart M, Cobbe N, Lee JY, McKay MJ, Orr-Weaver T, Heck MM, Sunkel CE (2000) The Drosophila RAD21 cohesin persists at the centromere region in mitosis. Curr Biol 10:1463–1466PubMedCrossRefGoogle Scholar
  61. Watanabe Y (2004) Modifying sister chromatid cohesion for meiosis. J Cell Sci 117:4017–4023PubMedCrossRefGoogle Scholar
  62. Watanabe Y, Nurse P (1999) Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400:461–464PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • A. Calvente
    • 1
    • 2
  • A. Viera
    • 1
  • M. T. Parra
    • 1
  • R. de la Fuente
    • 1
  • J. A. Suja
    • 1
  • J. Page
    • 1
  • J. L. Santos
    • 3
  • C. García de la Vega
    • 1
  • J. L. Barbero
    • 2
  • J. S. Rufas
    • 1
    Email author
  1. 1.Departamento de Biología, Facultad de Ciencias, Edificio de BiológicasUniversidad Autónoma de MadridMadridSpain
  2. 2.Departamento de Proliferación Celular y DesarrolloCentro de Investigaciones Biológicas (CSIC)MadridSpain
  3. 3.Departamento de Genética, Facultad de BiologíaUniversidad Complutense de MadridMadridSpain

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