Tying SUMO modifications to dynamic behaviors of chromosomes during meiotic prophase of Saccharomyces cerevisiae

Journal of Biomedical Science

Volumn 14, Issue 4, 2007, Pages 481-490

  Cheng, Chun Hsu ^a   Lin, Feng Ming ^a,b   Lo, Yu Hui ^a,b   Wang, Ting Fang ^a,b  

^a INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

Author keywords

Centromere; Homologous recombination; Meiosis; SUMO; Synaptonemal complex; Telomere

Indexed keywords

SUMO PROTEIN;

BUDDING; CHROMOSOME; CONFERENCE PAPER; ENZYME MODIFICATION; MEIOTIC PROPHASE I; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE;

BINDING SITES; CHROMOSOMES, FUNGAL; MEIOSIS; MODELS, BIOLOGICAL; PROPHASE; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN-PROTEIN LIGASES;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; SYNAPSIS;

EID: 34447330165     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1007/s11373-007-9176-0     Document Type: Conference Paper

References (79)

1. Zickler D., Kleckner N., 1998 The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32: 619-97
2. Zickler D., Kleckner N., 1999 Meiotic chromosomes: Integrating structure and function. Annu. Rev. Genet. 33: 603-754
3. Scherthan H., 2001 A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2: 621-7
4. Petronczki M., Siomos M.F., Nasmyth K., 2003 Un menage a quatre: The molecular biology of chromosome segregation in meiosis. Cell 112: 423-440
5. Hassold T., Hunt P., 2001 To err (meiotically) is human: The genesis of human aneuploidy. Nat. Rev. Genet. 2: 280-291
6. Burgess S.M., 2002 Homologous chromosome associations and nuclear order in meiotic and mitotically dividing cells of budding yeast. Adv. Genet. 46: 49-90
7. Loidl J., 2003 Chromosomes of the budding yeast Saccharomyces cerevisiae. Int. Rev. Cytol. 222: 141-196
8. Straight A.F., Marshall W.F., Sedat J.W., Murray A.W., 1997 Mitosis in living budding yeast: Anaphase A but no metaphase plate. Science 277: 574-578
9. Goshima G., Yanagida M., 2001 Time course analysis of precocious separation of sister centromeres in budding yeast: Continuously separated or frequently reassociated? Genes Cells 6: 765-773
10. He X., Asthana S., Sorger P.K., 2000 Transient sister chromatid separation and elastic deformation of chromosomes during mitosis in budding yeast. Cell 101: 763-775
11. Heun P., Taddei A., Gasser S.M., 2001 From snapshots to moving pictures: New perspectives on nuclear organization. Trends Cell Biol. 11: 519-525
12. Burgess S.M., Kleckner N., Weiner B.M., 1999 Somatic pairing of homologs in budding yeast: Existence and modulation. Genes Dev. 13: 1627-1641
13. Dekker J., Rippe K., Dekker M., Kleckner N., 2002 Capturing chromosome conformation. Science 295: 1306-1311
14. Keeney S., Giroux C.N., Kleckner N., 1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384
15. Bishop D.K., 1994 RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081-1092
16. Rockmill B., Sym M., Scherthan H., Roeder G.S., 1995 Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 9: 2684-2695
17. Gasior S.L., Wong A.K., Kora Y., Shinohara A., Bishop D.K., 1998 Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev 12: 2208-2221
18. Leu J.Y., Chua P.R., Roeder G.S., 1998 The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell 94: 375-386
19. Tsubouchi H., Roeder G.S., 2002 The Mnd1 protein forms a complex with hop2 to promote homologous chromosome pairing and meiotic double-strand break repair. Mol. Cell Biol. 22: 3078-3088
20. Peoples T.L., Dean E., Gonzalez O., Lambourne L., Burgess S.M., 2002 Close, stable homolog juxtaposition during meiosis in budding yeast is dependent on meiotic recombination, occurs independently of synapsis, and is distinct from DSB-independent pairing contacts. Genes Dev. 16: 1682-1695
21. Chen Y.K., Leng C.H., Olivares H., Lee M.H., Chang Y.C., Kung W.M., Ti S.C., Lo Y.H., Wang A.H., Chang C.S., Bishop D.K., Hsueh Y.P., Wang T.F., 2004 Heterodimeric complexes of Hop2 and Mnd1 function with Dmc1 to promote meiotic homolog juxtaposition and strand assimilation. Proc Natl Acad Sci USA 101: 10572-10577
22. Hayase A., Takagi M., Miyazaki T., Oshiumi H., Shinohara M., Shinohara A., 2004 A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell 119: 927-940
23. Tsubouchi H., Roeder G.S., 2004 The budding yeast mei5 and sae3 proteins act together with dmc1 during meiotic recombination. Genetics 168: 1219-1230
24. Peoples-Holst T.L., Burgess S.M., 2005 Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev. 19: 863-874
25. Lui D.Y., Peoples-Holst T.L., Mell J.C., Wu H.Y., Dean E.W., Burgess S.M., 2006 Analysis of close stable homolog juxtaposition during meiosis in mutants of Saccharomyces cerevisiae. Genetics 173: 1207-1222
26. Sym M., Engebrecht J.A., Roeder G.S., 1993 ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378
27. Tung K.S., Roeder G.S., 1998 Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149: 817-832
28. Dong H., Roeder G.S., 2000 Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J. Cell Biol. 148: 417-426
29. Page S.L., Hawley R.S., 2004 The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20: 525-558
30. Agarwal S., Roeder G.S., 2000 Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255
31. Chua P.R., Roeder G.S., 1998 Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359
32. Perry J., Kleckner N., Borner G.V., 2005 Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc. Natl. Acad. Sci. USA 102: 17594-17599
33. Tsubouchi T., Zhao H., Roeder G.S., 2006 The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev. Cell 10: 809-819
34. Fung J.C., Rockmill B., Odell M., Roeder G.S., 2004 Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116: 795-802
35. Borner G.V., Kleckner N., Hunter N., 2004 Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45
36. Laroche T., Martin S.G., Gotta M., Gorham H.C., Pryde F.E., Louis E.J., Gasser S.M., 1998 Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8: 653-656
37. Galy V., Olivo-Marin J.C., Scherthan H., Doye V., Rascalou N., Nehrbass U., 2000 Nuclear pore complexes in the organization of silent telomeric chromatin. Nature 403: 108-112
38. 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: 213-223
39. Conrad M.N., Dominguez A.M., Dresser M.E., 1997 Ndj1p, a meiotic telomere protein required for normal chromosome synapsis and segregation in yeast. Science 276: 1252-1255
40. Wu H.Y., Burgess S.M., 2006 Ndj1, a telomere-associated protein, promotes meiotic recombination in budding yeast. Mol. Cell Biol. 26: 3683-3694
41. Tsubouchi T., Roeder G.S., 2005 A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308: 870-873
42. Cheng C.H., Lo Y.H., Liang S.S., Ti S.C., Lin F.M., Yeh C.H., Huang H.Y., Wang T.F., 2006 SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae. Genes Dev. 20: 2067-2081
43. Hooker G.W., Roeder G.S., 2006 A role for SUMO in meiotic chromosome synapsis. Curr. Biol. 16: 1238-1243
44. Johnson E.S., 2004 Protein modification by SUMO. Annu. Rev. Biochem. 73: 355-382
45. Gill G., 2004 SUMO and ubiquitin in the nucleus: Different functions, similar mechanisms? Genes Dev. 18: 2046-2059
46. Muller S., Ledl A., Schmidt D., 2004 SUMO: A regulator of gene expression and genome integrity. Oncogene 23: 1998-2008
47. Reindle A., Belichenko I., Bylebyl G.R., Chen X.L., Gandhi N., Johnson E.S., 2006 Multiple domains in Siz SUMO ligases contribute to substrate selectivity. J. Cell Sci. 119: 4749-4757
48. Li S.J., Hochstrasser M., 2000 The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol. Cell Biol. 20: 2367-2377
49. Schwienhorst I., Johnson E.S., Dohmen R.J., 2000 SUMO conjugation and deconjugation. Mol. Gen. Genet. 263: 771-786
50. Li S.J., Hochstrasser M., 2003 The Ulp1 SUMO isopeptidase: Distinct domains required for viability, nuclear envelope localization, and substrate specificity. J. Cell Biol. 160: 1069-1081
51. Zhao X., Wu C.Y., Blobel G., 2004 Mlp-dependent anchorage and stabilization of a desumoylating enzyme is required to prevent clonal lethality. J. Cell Biol. 167: 605-611
52. Bachant J., Alcasabas A., Blat Y., Kleckner N., Elledge S.J., 2002 The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9: 1169-1182
53. Stead K., Aguilar C., Hartman T., Drexel M., Meluh P., Guacci V., 2003 Pds5p regulates the maintenance of sister chromatid cohesion and is sumoylated to promote the dissolution of cohesion. J. Cell Biol. 163: 729-741
54. Bylebyl G.R., Belichenko I., Johnson E.S., 2003 The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast. J. Biol. Chem. 278: 44113-441120
55. Shiio Y., Eisenman R.N., 2003 Histone sumoylation is associated with transcriptional repression. Proc. Natl. Acad. Sci. USA 100: 13225-13230
56. Sterner D.E., Nathan D., Reindle A., Johnson E.S., Berger S.L., 2006 Sumoylation of the yeast Gcn5 protein. Biochemistry 45: 1035-1042
57. Bencsath K.P., Podgorski M.S., Pagala V.R., Slaughter C.A., Schulman B.A., 2002 Identification of a multifunctional binding site on Ubc9p required for Smt3p conjugation. J. Biol. Chem. 277: 47938-47945
58. Takahashi Y., Toh E.A., Kikuchi Y., 2003 Comparative analysis of yeast PIAS-type SUMO ligases in vivo and in vitro. J. Biochem. (Tokyo) 133: 415-422
59. Johnson E.S., Gupta A.A., 2001 An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735-744
60. Taylor D.L., Ho J.C., Oliver A., Watts F.Z., 2002 Cell-cycle-dependent localisation of Ulp1, a Schizosaccharomyces pombe Pmt3 (SUMO)-specific protease. J. Cell Sci. 115: 1113-1122
61. Zhao X., Blobel G., 2005 A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. USA 102: 4777-4782
62. Shen T.H., Lin H.K., Scaglioni P.P., Yung T.M., Pandolfi P.P., 2006 The mechanisms of PML-nuclear body formation. Mol. Cell 24: 331-339
63. Lin D.Y., Huang Y.S., Jeng J.C., Kuo H.Y., Chang C.C., Chao T.T., Ho C.C., Chen Y.C., Lin T.P., Fang H.I., Hung C.C., Suen C.S., Hwang M.J., Chang K.S., Maul G.G., Shih H.M., 2006 Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 24: 341-354
64. Lee B.H., Yoshimatsu K., Maeda A., Ochiai K., Morimatsu M., Araki K., Ogino M., Morikawa S., Arikawa J., 2003 Association of the nucleocapsid protein of the Seoul and Hantaan hantaviruses with small ubiquitin-like modifier-1-related molecules. Virus Res. 98: 83-91
65. Kaukinen P., Vaheri A., Plyusnin A., 2003 Non-covalent interaction between nucleocapsid protein of Tula hantavirus and small ubiquitin-related modifier-1, SUMO-1. Virus Res. 92: 37-45
66. Wilson V.G., Rangasamy D., 2001 Viral interaction with the host cell sumoylation system. Virus Res. 81: 17-27
67. Hannich J.T., Lewis A., Kroetz M.B., Li S.J., Heide H., Emili A., Hochstrasser M., 2005 Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280: 4102-4110
68. Song J., Durrin L.K., Wilkinson T.A., Krontiris T.G., Chen Y., 2004 Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 101: 14373-14378
69. Smith A.V., Roeder G.S., 1997 The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136: 957-967
70. Smith K.N., Penkner A., Ohta K., Klein F., Nicolas A., 2001 B-type cyclins CLB5 and CLB6 control the initiation of recombination and synaptonemal complex formation in yeast meiosis. Curr. Biol. 11: 88-97
71. Henderson K.A., Keeney S., 2004 Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 101: 4519-4524
72. Pfander B., Moldovan G.L., Sacher M., Hoege C., Jentsch S., 2005 SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436: 428-433
73. Ulrich H.D., Vogel S., Davies A.A., 2005 SUMO keeps a check on recombination during DNA replication. Cell Cycle 4: 1699-1702
74. Montpetit B., Hazbun T.R., Fields S., Hieter P., 2006 Sumoylation of the budding yeast kinetochore protein Ndc10 is required for Ndc10 spindle localization and regulation of anaphase spindle elongation. J. Cell Biol. 174: 653-663
75. Takahashi Y., Yong-Gonzalez V., Kikuchi Y., Strunnikov A., 2006 SIZ1/SIZ2 control of chromosome transmission fidelity is mediated by the sumoylation of topoisomerase II. Genetics 172: 783-794
76. Potts P.R., Yu H., 2005 Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell Biol. 25: 7021-7032
77. Montelone B.A., Koelliker K.J., 1995 Interactions among mutations affecting spontaneous mutation, mitotic recombination, and DNA repair in yeast. Curr. Genet. 27: 102-109
78. Branzei D., Sollier J., Liberi G., Zhao X., Maeda D., Seki M., Enomoto T., Ohta K., Foiani M., 2006 Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127: 509-522
79. Jessop L., Rockmill B., Roeder G.S., Lichten M., 2006 Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genet. 2: e155