Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase i and by PATRONUS at interkinesis

Current Biology

Volumn 23, Issue 21, 2013, Pages 2090-2099

  Cromer, Laurence ^a   Jolivet, Sylvie ^a   Horlow, Christine ^a   Chelysheva, Liudmila ^a   Heyman, Jefri ^b,c   De Jaeger, Geert ^b,c   Koncz, Csaba ^d,e   De Veylder, Lieven ^b,c   Mercier, Raphael ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS;

ARABIDOPSIS PROTEIN; CELL CYCLE PROTEIN; PATRONUS PROTEIN, ARABIDOPSIS; SGO1 PROTEIN, ARABIDOPSIS; SGO2 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CENTROMERE; CHEMISTRY; CHROMOSOME SEGREGATION; CLASSIFICATION; CYTOLOGY; GENETICS; MEIOSIS; METABOLISM; MUTATION; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; CENTROMERE; CHROMOSOME SEGREGATION; MEIOSIS; MUTATION; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

EID: 84887146454     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.08.036     Document Type: Article

References (52)

1. K. Nasmyth, and C.H. Haering Cohesin: its roles and mechanisms Annu. Rev. Genet. 43 2009 525 558
2. F. Uhlmann, D. Wernic, M.A. Poupart, E.V. Koonin, and K. Nasmyth Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast Cell 103 2000 375 386
3. S. Hauf, I.C. Waizenegger, and J.M. Peters Cohesin cleavage by separase required for anaphase and cytokinesis in human cells Science 293 2001 1320 1323
4. J.-M. Peters, A. Tedeschi, and J. Schmitz The cohesin complex and its roles in chromosome biology Genes Dev. 22 2008 3089 3114
5. I.C. Waizenegger, S. Hauf, A. Meinke, and J.M. Peters Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase Cell 103 2000 399 410
6. S. Hauf, E. Roitinger, B. Koch, C.M. Dittrich, K. Mechtler, and J.-M. Peters Dissociation of cohesin from chromosome arms and loss of arm cohesion during early mitosis depends on phosphorylation of SA2 PLoS Biol. 3 2005 e69
7. S. Kueng, B. Hegemann, B.H. Peters, J.J. Lipp, A. Schleiffer, K. Mechtler, and J.-M. Peters Wapl controls the dynamic association of cohesin with chromatin Cell 127 2006 955 967
8. I. Sumara, E. Vorlaufer, P.T. Stukenberg, O. Kelm, N. Redemann, E.A. Nigg, and J.M. Peters The dissociation of cohesin from chromosomes in prophase is regulated by Polo-like kinase Mol. Cell 9 2002 515 525
9. T.S. Kitajima, S. Hauf, M. Ohsugi, T. Yamamoto, and Y. Watanabe Human Bub1 defines the persistent cohesion site along the mitotic chromosome by affecting Shugoshin localization Curr. Biol. 15 2005 353 359
10. B.E. McGuinness, T. Hirota, N.R. Kudo, J.-M. Peters, and K. Nasmyth Shugoshin prevents dissociation of cohesin from centromeres during mitosis in vertebrate cells PLoS Biol. 3 2005 e86
11. Z. Tang, H. Shu, W. Qi, N.A. Mahmood, M.C. Mumby, and H. Yu PP2A is required for centromeric localization of Sgo1 and proper chromosome segregation Dev. Cell 10 2006 575 585
12. D. Zickler, and N. Kleckner Meiotic chromosomes: integrating structure and function Annu. Rev. Genet. 33 1999 603 754
13. Y. Watanabe, and P. Nurse Cohesin Rec8 is required for reductional chromosome segregation at meiosis Nature 400 1999 461 464
14. F. Klein, P. Mahr, M. Galova, S.B. Buonomo, C. Michaelis, K. Nairz, and K. Nasmyth A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis Cell 98 1999 91 103
15. O. Hamant, I.N. Golubovskaya, R. Meeley, E. Fiume, L. Timofejeva, A. Schleiffer, K. Nasmyth, and W.Z. Cande A REC8-dependent plant Shugoshin is required for maintenance of centromeric cohesion during meiosis and has no mitotic functions Curr. Biol. 15 2005 948 954
16. M. Wang, D. Tang, K. Wang, Y. Shen, B. Qin, C. Miao, M. Li, and Z. Cheng OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis Plant J. 67 2011 583 594
17. T.S. Kitajima, S.A. Kawashima, and Y. Watanabe The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis Nature 427 2004 510 517
18. K.P. Rabitsch, J. Gregan, A. Schleiffer, J.-P. Javerzat, F. Eisenhaber, and K. Nasmyth Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II Curr. Biol. 14 2004 287 301
19. J. Lee, T.S. Kitajima, Y. Tanno, K. Yoshida, T. Morita, T. Miyano, M. Miyake, and Y. Watanabe Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells Nat. Cell Biol. 10 2008 42 52
20. E. Llano, R. Gómez, C. Gutiérrez-Caballero, Y. Herrán, M. Sánchez-Martín, L. Vázquez- Quiñones, T. Hernández, E. de Alava, A. Cuadrado, and J.L. Barbero Shugoshin-2 is essential for the completion of meiosis but not for mitotic cell division in mice Genes Dev. 22 2008 2400 2413
21. T. Ishiguro, K. Tanaka, T. Sakuno, and Y. Watanabe Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase Nat. Cell Biol. 12 2010 500 506
22. V.L. Katis, J.J. Lipp, R. Imre, A. Bogdanova, E. Okaz, B. Habermann, K. Mechtler, K. Nasmyth, and W. Zachariae Rec8 phosphorylation by casein kinase 1 and Cdc7-Dbf4 kinase regulates cohesin cleavage by separase during meiosis Dev. Cell 18 2010 397 409
23. C. Gutiérrez-Caballero, L.R. Cebollero, and A.M. Pendás Shugoshins: from protectors of cohesion to versatile adaptors at the centromere Trends Genet. 28 2012 1 10
24. I. d'Erfurth, S. Jolivet, N. Froger, O. Catrice, M. Novatchkova, M. Simon, E. Jenczewski, and R. Mercier Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains PLoS Genet. 4 2008 e1000274
25. I. d'Erfurth, S. Jolivet, N. Froger, O. Catrice, M. Novatchkova, and R. Mercier Turning meiosis into mitosis PLoS Biol. 7 2009 e1000124
26. M. Menges, L. Hennig, W. Gruissem, and J.A. Murray Genome-wide gene expression in an Arabidopsis cell suspension Plant Mol. Biol. 53 2003 423 442
27. N.P. Gauthier, L.J. Jensen, R. Wernersson, S. Brunak, and T.S. Jensen Cyclebase.org: version 2.0, an updated comprehensive, multi-species repository of cell cycle experiments and derived analysis results Nucleic Acids Res. 38 Database issue 2010 D699 D702
28. D. Ogawa, K. Abe, A. Miyao, M. Kojima, H. Sakakibara, M. Mizutani, H. Morita, Y. Toda, T. Hobo, and Y. Sato RSS1 regulates the cell cycle and maintains meristematic activity under stress conditions in rice Nat. Commun. 2 2011 278
29. J.M. Alonso, A.N. Stepanova, T.J. Leisse, C.J. Kim, H. Chen, P. Shinn, D.K. Stevenson, J. Zimmerman, P. Barajas, and R. Cheuk Genome-wide insertional mutagenesis of Arabidopsis thaliana Science 301 2003 653 657
30. M.P. Alexander Differential staining of aborted and nonaborted pollen Stain Technol. 44 1969 117 122
31. S.J. Robinson, L.H. Tang, B.A. Mooney, S.J. McKay, W.E. Clarke, M.G. Links, S. Karcz, S. Regan, Y.-Y. Wu, and M.Y. Gruber An archived activation tagged population of Arabidopsis thaliana to facilitate forward genetics approaches BMC Plant Biol. 9 2009 101
32. G. Ríos, A. Lossow, B. Hertel, F. Breuer, S. Schaefer, M. Broich, T. Kleinow, J. Jásik, J. Winter, and A. Ferrando Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes Plant J. 32 2002 243 253
33. X. Cai, F. Dong, R.E. Edelmann, and C.A. Makaroff The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing J. Cell Sci. 116 2003 2999 3007
34. A.M. Bhatt, C. Lister, T. Page, P. Fransz, K. Findlay, G.H. Jones, H.G. Dickinson, and C. Dean The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family Plant J. 19 1999 463 472
35. L. Chelysheva, S. Diallo, D. Vezon, G. Gendrot, N. Vrielynck, K. Belcram, N. Rocques, A. Márquez-Lema, A.M. Bhatt, and C. Horlow AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis J. Cell Sci. 118 2005 4621 4632
36. Z. Liu, and C.A. Makaroff Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis Plant Cell 18 2006 1213 1225
37. P.B. Talbert, R. Masuelli, A.P. Tyagi, L. Comai, and S. Henikoff Centromeric localization and adaptive evolution of an arabidopsis histone H3 variant Plant Cell 14 2002 1053 1066
38. A. Sessions, E. Burke, G. Presting, G. Aux, J. McElver, D. Patton, B. Dietrich, P. Ho, J. Bacwaden, and C. Ko A high-throughput Arabidopsis reverse genetics system Plant Cell 14 2002 2985 2994
39. J. Van Leene, H. Stals, D. Eeckhout, G. Persiau, E. Van De Slijke, G. Van Isterdael, A. De Clercq, E. Bonnet, K. Laukens, and N. Remmerie A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana Mol. Cell. Proteomics 6 2007 1226 1238
40. J. Van Leene, E. Witters, D. Inzé, and G. De Jaeger Boosting tandem affinity purification of plant protein complexes Trends Plant Sci. 13 2008 517 520
41. J. Van Leene, D. Eeckhout, G. Persiau, E. Van De Slijke, J. Geerinck, G. Van Isterdael, E. Witters, and G. De Jaeger Isolation of transcription factor complexes from Arabidopsis cell suspension cultures by tandem affinity purification Methods Mol. Biol. 754 2011 195 218
42. J. Van Leene, J. Hollunder, D. Eeckhout, G. Persiau, E. Van De Slijke, H. Stals, G. Van Isterdael, A. Verkest, S. Neirynck, and Y. Buffel Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana Mol. Syst. Biol. 6 2010 397
43. J. Heyman, H. Van den Daele, K. De Wit, V. Boudolf, B. Berckmans, A. Verkest, C.L. Alvim Kamei, G. De Jaeger, C. Koncz, and L. De Veylder Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome Plant Cell 23 2011 4394 4410
44. A. Salic, J.C. Waters, and T.J. Mitchison Vertebrate shugoshin links sister centromere cohesion and kinetochore microtubule stability in mitosis Cell 118 2004 567 578
45. J.A. Pesin, and T.L. Orr-Weaver Regulation of APC/C activators in mitosis and meiosis Annu. Rev. Cell Dev. Biol. 24 2008 475 499
46. Z. Kevei, M. Baloban, O. Da Ines, H. Tiricz, A. Kroll, K. Regulski, P. Mergaert, and E. Kondorosi Conserved CDC20 cell cycle functions are carried out by two of the five isoforms in Arabidopsis thaliana PLoS ONE 6 2011 e20618
47. K. Nasmyth Cohesin: a catenase with separate entry and exit gates? Nat. Cell Biol. 13 2011 1170 1177
48. J. Vignard, T. Siwiec, L. Chelysheva, N. Vrielynck, F. Gonord, S.J. Armstrong, P. Schlögelhofer, and R. Mercier The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana PLoS Genet. 3 2007 1894 1906
49. T. Nakagawa, T. Kurose, T. Hino, K. Tanaka, M. Kawamukai, Y. Niwa, K. Toyooka, K. Matsuoka, T. Jinbo, and T. Kimura Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation J. Biosci. Bioeng. 104 2007 34 41
50. S.J. Clough, and A.F. Bent Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Plant J. 16 1998 735 743
51. Y. Azumi, D. Liu, D. Zhao, W. Li, G. Wang, Y. Hu, and H. Ma Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein EMBO J. 21 2002 3081 3095
52. L. Chelysheva, L. Grandont, N. Vrielynck, S. le Guin, R. Mercier, and M. Grelon An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1 Cytogenet. Genome Res. 129 2010 143 153