SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe

Chromosoma

Volumn 119, Issue 1, 2010, Pages 59-72

  Spirek, Mario ^a,b   Estreicher, Anna ^a   Csaszar, Edina ^a   Wells, Jennifer ^c   McFarlane, Ramsay J ^c   Watts, Felicity Z ^d   Loidl, Josef ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b MASARYK UNIVERSITY   (Czech Republic)

^c BANGOR UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PROTEIN HOP1; PROTEIN PLI1; PROTEIN PMT3; PROTEIN REC10; PROTEIN REC25; PROTEIN REC27; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FUNGAL DEVELOPMENT; GENE MUTATION; GENETIC RECOMBINATION; MEIOSIS; MITOTIC RECOMBINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SUMOYLATION; UBIQUITINATION; WILD TYPE;

CHROMOSOME PAIRING; CHROMOSOMES, FUNGAL; MEIOSIS; RECOMBINATION, GENETIC; REPRESSOR PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 74049100854     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-009-0241-5     Document Type: Article

References (46)

1. S Agarwal GS Roeder 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins Cell 102 245 255 10.1016/S0092- 8674(00)00029-5 1:CAS:528:DC%2BD3cXltl2hs74%3D 10943844
2. J Bähler T Wyler J Loidl J Kohli 1993 Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis J Cell Biol 121 241 256 10.1083/jcb.121.2.241 8468345
3. J Bähler JQ Wu MS Longtine NG Shah A Mckenzie AB Steever A Wach P Philippsen JR Pringle 1998 Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe Yeast 14 943 951 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y 9717240 (Pubitemid 28328000)
4. JA Carballo AL Johnson SG Sedgwick RS Cha 2008 Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination Cell 132 758 770 10.1016/j.cell.2008.01.035 1:CAS:528: DC%2BD1cXjs1aitrs%3D 18329363 (Pubitemid 351312803)
5. MD Cervantes JA Farah GR Smith 2000 Meiotic DNA breaks associated with recombination in S. pombe Mol Cell 5 883 888 10.1016/S1097-2765(00)80328-7 1:CAS:528:DC%2BD3cXjsl2ku7k%3D 10882124
6. C-H Cheng Y-H Lo S-S Liang S-C Ti F-M Lin C-H Yeh H-Y Huang T-F Wang 2006 SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae Genes Dev 20 2067 2081 10.1101/gad.1430406 1:CAS:528:DC%2BD28XosVeltLk%3D 16847351 (Pubitemid 44157458)
7. C-H Cheng F-M Lin Y-H Lo T-F Wang 2007 Tying SUMO modifications to dynamic behaviors of chromosomes during meiotic prophase of Saccharomyces cerevisiae J Biomed Sci 14 481 490 10.1007/s11373-007-9176-0 1:CAS:528:DC%2BD2sXpslGrsrw%3D 17530453 (Pubitemid 47063486)
8. L Davis AE Rozalén S Moreno GR Smith C Martín-Castellanos 2008 Rec25 and Rec27, novel linear-element components, link cohesin to meiotic DNA breakage and recombination Curr Biol 18 849 854 10.1016/j.cub.2008.05.025 1:CAS:528:DC%2BD1cXmsFymtLk%3D 18514516
9. D-Q Ding N Sakurai Y Katou T Itoh K Shirahige T Haraguchi Y Hiraoka 2006 Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast J Cell Biol 174 499 508 10.1083/jcb.200605074 1:CAS:528: DC%2BD28XosVKgt70%3D 16893973 (Pubitemid 44231862)
10. C Ellermeier GR Smith 2005 Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe Proc Natl Acad Sci USA 102 10952 10957 10.1073/pnas.0504805102 1:CAS:528:DC%2BD2MXnvVWjtbg%3D 16043696 (Pubitemid 41105974)
11. SL Forsburg N Rhind 2006 Basic methods for fission yeast Yeast 23 173 183 10.1002/yea.1347 1:CAS:528:DC%2BD28XjtVOhu70%3D 16498704
12. J Gregan PK Rabitsch B Sakem O Csutak V Latypov E Lehmann J Kohli K Nasmyth 2005 Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast Curr Biol 15 1663 1669 10.1016/j.cub.2005.07.059 1:CAS:528:DC%2BD2MXhtVWnsLjN 16169489 (Pubitemid 41323745)
13. Gutz H, Heslot H, Leupold U, Loprieno N (1974) Schizosaccharomyces pombe. Handbook of Genetics. pp. 395-446
14. KA Henderson S Keeney 2004 Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks Proc Natl Acad Sci USA 101 4519 4524 10.1073/pnas.0400843101 1:CAS:528:DC%2BD2cXjtFKisrg%3D 15070750 (Pubitemid 38437443)
15. A Hirata K Tanaka 1982 Nuclear behavior during conjugation and meiosis in the fission yeast Schizosaccharomyces pombe J Gen Appl Microbiol 28 263 274 10.2323/jgam.28.263
16. JCY Ho NJ Warr H Shimizu FZ Watts 2001 SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52 Nucleic Acids Res 29 4179 4186 10.1093/nar/29.20.4179 1:CAS:528:DC%2BD3MXotlWguro%3D 11600706
17. GW Hooker GS Roeder 2006 A role for SUMO in meiotic chromosome synapsis Curr Biol 16 1238 1243 10.1016/j.cub.2006.04.045 1:CAS:528:DC%2BD28XlvF2jtLw%3D 16782016 (Pubitemid 43867294)
18. A Keller AI Nesvizhskii E Kolker R Aebersold 2002 Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal Chem 74 5383 5392 10.1021/ac025747h 1:CAS:528: DC%2BD38XmvVyktL4%3D 12403597 (Pubitemid 35215372)
19. F Klein T Laroche ME Cardenas JFX Hofmann D Schweizer SM Gasser 1992 Localization of RAP1 and topoisomerase II in nuclei and meiotic chromosomes of yeast J Cell Biol 117 935 948 10.1083/jcb.117.5.935 1:CAS:528:DyaK38XitlWntb0%3D 1315786
20. F Klein P Mahr M Galova SBC Buonomo C Michaelis K Nairz K Nasmyth 1999 A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis Cell 98 91 103 10.1016/S0092-8674(00)80609-1 1:CAS:528:DyaK1MXks1Kktr0%3D 10412984 (Pubitemid 29331199)
21. A Koshiyama FN Hamada SH Namekawa K Iwabata H Sugawara A Sakamoto T Ishizaki K Sakaguchi 2006 Sumoylation of a meiosis-specific RecA homolog, Lim15/Dmc1, via interaction with the small ubiquitin-related modifier (SUMO)-conjugating enzyme Ubc9 FEBS J 273 4003 4012 10.1111/j.1742-4658.2006. 05403.x 1:CAS:528:DC%2BD28XhtVWgs7fI 16879611 (Pubitemid 44253654)
22. J Loidl 2006 S. pombe linear elements: the modest cousins of synaptonemal complexes Chromosoma 115 260 271 10.1007/s00412-006-0047-7 16532354
23. A Lorenz JL Wells DW Pryce M Novatchkova F Eisenhaber RJ McFarlane J Loidl 2004 S. pombe meiotic linear elements contain proteins related to synaptonemal complex components J Cell Sci 117 3343 3351 10.1242/jcs.01203 1:CAS:528:DC%2BD2cXms1ensLc%3D 15226405 (Pubitemid 39139918)
24. A Lorenz A Estreicher J Kohli J Loidl 2006 Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe Chromosoma 115 330 340 10.1007/s00412-006-0053-9 1:CAS:528:DC%2BD28XmtVyjt7g%3D 16532353 (Pubitemid 43923359)
25. C Martín-Castellanos M Blanco AE Rozalén L Pérez-Hidalgo AI García F Conde J Mata C Ellermeier L Davis PA San Segundo GR Smith S Moreno 2005 A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events Curr Biol 15 2056 2062 10.1016/j.cub.2005.10.038 16303567 (Pubitemid 41654631)
26. J Mata R Lyne G Burns J Bähler 2002 The transcriptional program of meiosis and sporulation in fission yeast Nat Genet 32 143 147 10.1038/ng951 1:CAS:528:DC%2BD38Xms1ajsL8%3D 12161753 (Pubitemid 34977209)
27. M Molnar J Bähler M Sipiczki M Kohli 1995 The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis Genetics 141 61 73 1:CAS:528:DyaK28Xht1CmsbY%3D 8536990
28. M Molnar E Doll A Yamamoto Y Hiraoka J Kohli 2003 Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing J Cell Sci 116 1719 1731 10.1242/jcs.00387 1:CAS:528: DC%2BD3sXktVGgt7s%3D 12665553 (Pubitemid 36582159)
29. P Munz 1994 An analysis of interference in the fission yeast Schizosaccharomyces pombe Genetics 137 701 707 1:CAS:528:DyaK2MXjsFSrtw%3D%3D 8088515
30. AI Nesvizhskii A Keller E Kolker R Aebersold 2003 A statistical model for identifying proteins by tandem mass spectrometry Anal Chem 75 4646 4658 10.1021/ac0341261 1:CAS:528:DC%2BD3sXltlynt70%3D 14632076 (Pubitemid 37082259)
31. H Niu E Job C Park D Moazed SP Gygi NM Hollingsworth 2007 Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis Mol Cell Biol 27 5456 5467 10.1128/MCB.00416-07 1:CAS:528:DC%2BD2sXoslKru7Y%3D 17526735 (Pubitemid 47124398)
32. G Octobre A Lorenz J Loidl J Kohli 2008 The Rad52 homologs Rad22 and Rti1 of Schizosaccharomyces pombe are not essential for meiotic interhomolog recombination, but are required for meiotic intrachromosomal recombination and mating-type-related DNA repair Genetics 178 2399 2412 10.1534/genetics.107. 085696 1:CAS:528:DC%2BD1cXmt1eksro%3D 18430957
33. LW Olson U Edén ME Mitani R Egel 1978 Asynaptic meiosis in fission yeast? Hereditas 89 189 199 10.1111/j.1601-5223.1978.tb01275.x
34. F Osman J Dixon CL Doe MC Whitby 2003 Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis Mol Cell 12 761 774 10.1016/S1097-2765(03)00343-5 1:CAS:528:DC%2BD3sXnvFGrt7k%3D 14527420 (Pubitemid 37222495)
35. DW Pryce RJ McFarlane 2009 The meiotic recombination hot spots of Schizosaccharomyces pombe Genome Dyn Stab 5 1 13 10.1159/000166614 1:CAS:528:DC%2BD1MXhslWiurs%3D
36. DW Pryce A Lorenz JB Smirnova J Loidl RJ McFarlane 2005 Differential activation of M26-containing meiotic recombination hot spots in Schizosaccharomyces pombe Genetics 170 95 106 10.1534/genetics.104.036301 1:CAS:528:DC%2BD2MXlslKktbo%3D 15744055 (Pubitemid 40799974)
37. G Rigaut A Shevchenko B Rutz M Wilm M Mann B Séraphin 1999 A generic protein purification method for protein complex characterization and proteome exploration Nat Biotech 17 1030 1032 10.1038/13732 1:CAS:528: DyaK1MXmvVelsbs%3D (Pubitemid 29474865)
38. M Sacher B Pfander C Hoege S Jentsch 2006 Control of Rad52 recombination activity by double-strand break-induced SUMO modification Nature Cell Biol 8 1284 1290 10.1038/ncb1488 1:CAS:528:DC%2BD28XhtFCqu7jJ 17013376 (Pubitemid 44660594)
39. M Sato S Dhut T Toda 2005 New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe Yeast 22 583 591 10.1002/yea.1233 1:CAS:528:DC%2BD2MXmsVars7c%3D 15942936 (Pubitemid 40932159)
40. A Shevchenko A Roguev D Schaft L Buchanan B Habermann C Sakalar H Thomas NJ Krogan A Shevchenko AF Stewart 2008 Chromatin Central: towards the comparative proteome by accurate mapping of the yeast proteomic environment Genome Biol 9 R167 10.1186/gb-2008-9-11-r167 19040720
41. K Spink JCY Ho K Tanaka FZ Watts A Chambers 2005 The telomere-binding protein Taz1p as a target for modification by a SUMO-1 homologue in fission yeast Biochem Genet 43 103 117 10.1007/s10528-005-1503-4 1:CAS:528: DC%2BD2MXisV2htLg%3D 15932060 (Pubitemid 40543708)
42. JJ Tasto RH Carnahan WH McDonald KL Gould 2001 Vectors and gene targeting modules for tandem affinity purification in Schizosaccharomyces pombe Yeast 18 657 662 10.1002/yea.713 1:CAS:528:DC%2BD3MXjvFKjtL0%3D 11329175 (Pubitemid 32496341)
43. FZ Watts 2007 The role of SUMO in chromosome segregation Chromosoma 116 15 20 10.1007/s00412-006-0079-z 17031663 (Pubitemid 46179018)
44. FZ Watts A Skilton JCY Ho LK Boyd MAM Trickey L Gardner FX Ogi EA Outwin 2007 The role of Schizosaccharomyces pombe SUMO ligases in genome stability Biochem Soc Trans 35 1379 1384 10.1042/BST0351379 1:CAS:528:DC%2BD2sXhtlGmtL7E 18031226
45. JL Wells DW Pryce A Estreicher J Loidl RJ McFarlane 2006 Linear element-independent meiotic recombination in Schizosaccharomyces pombe Genetics 174 1105 1114 10.1534/genetics.106.063818 1:CAS:528:DC%2BD2sXktlChtg%3D%3D 16980386 (Pubitemid 44808286)
46. D Zickler N Kleckner 1999 Meiotic chromosomes: integrating structure and function Annu Rev Genet 33 603 754 10.1146/annurev.genet.33.1.603 1:CAS:528:DC%2BD3cXhtVSmsL4%3D 10690419 (Pubitemid 30083134)