Global SUMO proteome responses guide gene regulation, mRNA biogenesis, and plant stress responses

Frontiers in Plant Science

Volumn 3, Issue SEP, 2012, Pages

  Mazur, Magdalena J ^a   van den Burg, Harrold A ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Acetylation; Chromatin; Heat shock; Histones; Stress; SUMO

Indexed keywords

EID: 84889079202     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00215     Document Type: Review

References (115)

1. Abed, M., Barry, K. C., Kenyagin, D., Koltun, B., Phippen, T. M., Delrow, J. J., Parkhurst, S. M., and Orian, A. (2011). Degringolade, a SUMO-targeted ubiquitin ligase, inhibits hairy/groucho-mediated repression. EMBO J. 30, 1289-1301.
2. Ahn, J. W., Lee, Y. A., Ahn, J. H., and Choi, C. Y. (2009). Covalent conjugation of groucho with SUMO-1 modulates its corepressor activity. Biochem. Biophys. Res. Commun. 379, 160-165.
3. Aichinger, E., Villar, C. B. R., Farrona, S., Reyes, J. C., Hennig, L., and Kohler, C. (2009). CHD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet. 5, e1000605. doi: 10.1371/journal.pgen.1000605
4. Anckar, J., and Sistonen, L. (2007). SUMO: getting it on. Biochem. Soc. Trans. 35, 1409-1413.
5. Arabidopsis Interactome Mapping Consortium. (2011). Evidence for network evolution in an Arabidopsis interactome map. Science 333, 601-607.
6. Ausin, I., Alonso-Blanco, C., Jarillo, J. A., Ruiz-Garcia, L., and Martinez-Zapater, J. M. (2004). Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat. Genet. 36, 162-166.
7. Baron, R., and Vellore, N. A. (2012). LSD1/CoREST Reversible opening-closing dynamics: discovery of a nanoscale clamp for chromatin and protein binding. Biochemistry 51, 3151-3153.
8. Bauer, D. C., Buske, F. A., and Bailey, T. L. (2010). Dual-functioning transcription factors in the developmental gene network of Drosophila melanogaster. BMC Bioinformatics 11, 366. doi:10.1186/1471-2105-11-366
9. Benhamed, M., Martin-Magniette, M. L., Taconnat, L., Bitton, F., Servet, C., De Clercq, R., De Meyer, B., Buysschaert, C., Rombauts, S., Villarroel, R., Aubourg, S., Beynon, J., Bhalerao, R. P., Coupland, G., Gruissem, W., Menke, F. L. H., Weisshaar, B., Renou, J. P., Zhou, D. X., and Hilson, P. (2008). Genome-scale Arabidopsis promoter array identifies targets of the histone acetyltransferase GCN5. Plant J. 56, 493-504.
10. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. (2002). Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356.
11. Blomster, H. A., Hietakangas, V., Wu, J., Kouvonen, P., Hautaniemi, S., and Sistonen, L. (2009). Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites. Mol. Cell. Proteomics 8, 1382-1390.
12. Blomster, H. A., Imanishi, S. Y., Siimes, J., Kastu, J., Morrice, N. A., Eriksson, J. E., and Sistonen, L. (2010). In vivo identification of sumoylation sites by a signature tag and cysteine-targeted affinity purification. J. Biol. Chem. 285, 19324-19329.
13. Bruderer, R., Tatham, M. H., Plechanovova, A., Matic, I., Garg, A. K., and Hay, R. T. (2011). Purification and identification of endogenous poly SUMO conjugates. EMBO Rep. 12, 142-148.
14. Budhiraja, R., Hermkes, R., Muller, S., Schmidt, J., Colby, T., Panigrahi, K., Coupland, G., and Bachmair, A. (2009). Substrates related to chromatin and to RNA-dependent processes are modified by Arabidopsis SUMO isoforms that differ in a conserved residue with influence on desumoylation. Plant Physiol. 149, 1529-1540.
15. Castano-Miquel, L., Segui, J., and Lois, L. M. (2011). Distinctive properties of Arabidopsis SUMO paralogues support the in vivo predominant role of AtSUMO1/2 isoforms. Biochem. J. 436, 581-590.
16. Castro, P. H., Tavares, R. M., Bejarano, E. R., and Azevedo, H. (2012). SUMO, a heavyweight player in plant abiotic stress responses. Cell. Mol. Life Sci.
17. Catala, R., Ouyang, J., Abreu, I. A., Hu, Y., Seo, H., Zhang, X., and Chua, N. H. (2007). The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19, 2952-2966.
18. Causier, B., Ashworth, M., Guo, W., and Davies, B. (2012). The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 158, 423-438.
19. Cheema, A., Knights, C. D., Rao, M., Catania, J., Perez, R., Simons, B., Dakshanamurthy, S., Kolukula, V. K., Tilli, M., Furth, P. A., Albanese, C., and Avantaggiati, M. L. (2010). Functional mimicry of the acetylated C-terminal tail of p53 by a SUMO-1 acetylated domain, SAD. J. Cell. Physiol. 225, 371-384.
20. Colby, T., Matthai, A., Boeckelmann, A., and Stuible, H. P. (2006). SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol. 142, 318-332.
21. David, G., Neptune, M. A., and Depinho, R. A. (2002). SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J. Biol. Chem. 277, 23658-23663.
22. Deal, R. B., and Henikoff, S. (2011). The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat. Protoc. 6, 56-68.
23. Denison, C., Rudner, A. D., Gerber, S. A., Bakalarski, C. E., Moazed, D., and Gygi, S. P. (2005). A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol. Cell. Proteomics 4, 246-254.
24. Denuc, A., and Marfany, G. (2010). SUMO and ubiquitin paths converge. Biochem. Soc. Trans. 38, 34-39.
25. Elrouby, N., and Coupland, G. (2010). Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc. Natl. Acad. Sci. U.S.A. 107, 17415-17420.
26. Emanuele, M. J., Elia, A. E. H., Xu, Q., Thoma, C. R., Izhar, L., Leng, Y., Guo, A., Chen, Y. N., Rush, J., Hsu, P. W. C., Yen, H. C. S., and Elledge, S. J. (2011). Global identification of modular cullin-RING ligase substrates. Cell 147, 459-474.
27. Galisson, F., Mahrouche, L., Courcelles, M., Bonneil, E., Meloche, S., Chelbi-Alix, M. K., and Thibault, P. (2011). A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol. Cell. Proteomics 10, M110004796.
28. Ganesan, A. K., Kho, Y., Kim, S. C., Chen, Y., Zhao, Y., and White, M. A. (2007). Broad spectrum identification of SUMO substrates in melanoma cells. Proteomics 7, 2216-2221.
29. Garcia-Dominguez, M., March-Diaz, R., and Reyes, J. C. (2008). The PHD domain of plant PIAS proteins mediates sumoylation of bromodomain GTE proteins. J. Biol. Chem. 283, 21469-21477.
30. Garcia-Dominguez, M., and Reyes, J. C. (2009). SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim. Biophys. Acta 1789, 451-459.
31. Gocke, C. B., and Yu, H. (2008). ZNF198 stabilizes the LSD1-CoREST-HDAC1 complex on chromatin through its MYM-type zinc fingers. PLoS ONE 3, e3255. doi:10.1371/journal.pone.0003255
32. Golebiowski, F., Matic, I., Tatham, M. H., Cole, C., Yin, Y., Nakamura, A., Cox, J., Barton, G. J., Mann, M., and Hay, R. T. (2009). System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2, ra24.
33. Gonzalez, D., Bowen, A. J., Carroll, T. S., and Conlan, R. S. (2007). The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol. Cell Biol. 27, 5306-5315.
34. Gu, X., Jiang, D., Yang, W., Jacob, Y., Michaels, S. D., and He, Y. (2011). Arabidopsis homologs of retinoblastoma-associated protein 46/48 associate with a histone deacetylase to act redundantly in chromatin silencing. PLoS Genet. 7, e1002366. doi:10.1371/journal.pgen.1002366
35. Hannich, J. T., Lewis, A., Kroetz, M. B., Li, S. J., Heide, H., Emili, A., and Hochstrasser, M. (2005). Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 280, 4102-4110.
36. He, Y., Michaels, S. D., and Amasino, R. M. (2003). Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751-1754.
37. Hsiao, H. H., Meulmeester, E., Frank, B. T. C., Melchior, F., and Urlaub, H. (2009). "ChopNspice, " a mass-spectrometric approach that allows identification of endogenous SUMO-conjugated peptides. Mol. Cell. Proteomics2664-2675.
38. Ishida, T., Fujiwara, S., Miura, K., Stacey, N., Yoshimura, M., Schneider, K., Adachi, S., Minamisawa, K., Umeda, M., and Sugimoto, K. (2009). SUMO E3 Ligase HIGH PLOIDY2 Regulates Endocycle Onset and Meristem Maintenance in Arabidopsis. Plant Cell 21, 2284-2297.
39. Ivanov, A. V., Peng, H., Yurchenko, V., Yap, K. L., Negorev, D. G., Schultz, D. C., Psulkowski, E., Fredericks, W. J., White, D. E., Maul, G. G., Sadofsky, M. J., Zhou, M. M., and Rauscher, F. J. III. (2007). PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol. Cell 28, 823-837.
40. Jennings, B. H., and Ish-Horowicz, D. (2008). The groucho/TLE/Grg family of transcriptional co-repressors. Genome Biol. 9, 205.
41. Jeon, J., and Kim, J. (2011). FVE, an Arabidopsis homologue of the retinoblastoma-associated protein that regulates flowering time and cold response, binds to chromatin as a large multiprotein complex. Mol. Cells 32, 227-234.
42. Jeram, S. M., Srikumar, T., Zhang, X. D., Anne Eisenhauer, H., Rogers, R., Pedrioli, P. G. A., Matunis, M., and Raught, B. (2010). An improved SUMmOn-based methodology for the identification of ubiquitin and ubiquitin-like protein conjugation sites identifies novel ubiquitin-like protein chain linkages. Proteomics 10, 254-265.
43. Jin, J. B., Jin, Y. H., Lee, J., Miura, K., Yoo, C. Y., Kim, W. Y., Van Oosten, M., Hyun, Y., Somers, D. E., Lee, I., Yun, D. J., Bressan, R. A., and Hasegawa, P. M. (2008). The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J. 53, 530-540.
44. Kagale, S., and Rozwadowski, K. (2011). EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6, 141-146.
45. Kaminsky, R., Denison, C., Bening-Abu-Shach, U., Chisholm, A. D., Gygi, S. P., and Broday, L. (2009). SUMO regulates the assembly and function of a cytoplasmic intermediate filament protein in C. elegans. Dev. Cell 17, 724-735.
46. Kerscher, O. (2007). SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 8, 550-555.
47. Kim, H. J., Hyun, Y., Park, J. Y., Park, M. J., Park, M. K., Kim, M. D., Lee, M. H., Moon, J., Lee, I., and Kim, J. (2004). A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat. Genet. 36, 167-171.
48. Kim, W., Bennett, E. J., Huttlin, E. L., Guo, A., Li, J., Possemato, A., Sowa, M. E., Rad, R., Rush, J., Comb, M. J., Harper, J. W., and Gygi, S. P. (2011). Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 44, 325-340.
49. Kunert, N., and Brehm, A. (2009). Novel Mi-2 related ATP-dependent chromatin remodelers. Epigenetics 4, 209-211.
50. Kunert, N., Wagner, E., Murawska, M., Klinker, H., Kremmer, E., and Brehm, A. (2009). dMec: a novel Mi-2 chromatin remodelling complex involved in transcriptional repression. EMBO J. 28, 533-544.
51. Kurepa, J., Walker, J. M., Smalle, J., Gosink, M. M., Davis, S. J., Durham, T. L., Sung, D. Y., and Vierstra, R. D. (2003). The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and-2 conjugates is increased by stress. J. Biol. Chem. 278, 6862-6872.
52. Lee, J. E., and Golz, J. F. (2012). Diverse roles of Groucho/Tup1 co-repressors in plant growth and development. Plant Signal. Behav. 7, 86-92.
53. Li, T., Evdokimov, E., Shen, R. F., Chao, C. C., Tekle, E., Wang, T., Stadtman, E. R., Yang, D. C. H., and Chock, P. B. (2004). Sumoylation of heterogeneous nuclear ribonucleoproteins, zinc finger proteins, and nuclear pore complex proteins: a proteomic analysis. Proc. Natl. Acad. Sci. U.S.A. 101, 8551-8556.
54. Liu, Z., and Karmarkar, V. (2008). Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci. 13, 137-144.
55. Loyola, A., and Almouzni, G. (2004). Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta 1677, 3-11.
56. Makhnevych, T., Sydorskyy, Y., Xin, X., Srikumar, T., Vizeacoumar, F. J., Jeram, S. M., Li, Z., Bahr, S., Andrews, B. J., Boone, C., and Raught, B. (2009). Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol. Cell 33, 124-135.
57. Mao, Y., Pavangadkar, K. A., Thomashow, M. F., and Triezenberg, S. J. (2006). Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim. Biophys. Acta 1759, 69-79.
58. Martin, N., Schwamborn, K., Schreiber, V., Werner, A., Guillier, C., Zhang, X. D., Bischof, O., Seeler, J. S., and Dejean, A. (2009). PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 28, 3534-3548.
59. Matafora, V., D'amato, A., Mori, S., Blasi, F., and Bachi, A. (2009). Proteomics analysis of nucleolar SUMO-1 target proteins upon proteasome inhibition. Mol. Cell. Proteomics 8, 2243-2255.
60. Matic, I., Schimmel, J., Hendriks, I. A., Van Santen, M. A., Van De Rijke, F., Van Dam, H., Gnad, F., Mann, M., and Vertegaal, A. C. O. (2010). Site-specific identification of SUMO-2 targets in cells reveals an inverted SUMOylation motif and a hydrophobic cluster SUMOylation motif. Mol. Cell 39, 641-652.
61. McDonel, P., Costello, I., and Hendrich, B. (2009). Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development. Int. J. Biochem. Cell Biol. 41, 108-116.
62. Meier, I. (2012). mRNA export and sumoylation-lessons from plants. Biochim. Biophys. Acta, 531-537.
63. Messner, S., Schuermann, D., Altmeyer, M., Kassner, I., Schmidt, D., Schar, P., Muller, S., and Hottiger, M. O. (2009). Sumoylation of poly(ADP-ribose) polymerase 1 inhibits its acetylation and restrains transcriptional coactivator function. FASEB J. 23, 3978-3989.
64. Miller, M. J., Barrett-Wilt, G. A., Hua, Z., and Vierstra, R. D. (2010). Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A.107, 16512-16517.
65. Miller, M. J., and Vierstra, R. D. (2011). Mass spectrometric identification of SUMO substrates provides insights into heat stress-induced SUMOylation in plants. Plant Signal. Behav. 6, 130-133.
66. Miura, K., Jin, J. B., Lee, J., Yoo, C. Y., Stirm, V., Miura, T., Ashworth, E. N., Bressan, R. A., Yun, D. J., and Hasegawa, P. M. (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19, 1403-1414.
67. Mossessova, E., and Lima, C. D. (2000). Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5, 865-876.
68. Mujtaba, S., Zeng, L., and Zhou, M. M. (2007). Structure and acetyl-lysine recognition of the bromodomain. Oncogene 26, 5521-5527.
69. Mukhopadhyay, D., and Dasso, M. (2007). Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 32, 286-295.
70. Murtas, G., Reeves, P. H., Fu, Y. F., Bancroft, I., Dean, C., and Coupland, G. (2003). A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of small ubiquitin-related modifier conjugates. Plant Cell 15, 2308-2319.
71. Murzina, N. V., Pei, X. Y., Zhang, W., Sparkes, M., Vicente-Garcia, J., Pratap, J. V., Mclaughlin, S. H., Ben-Shahar, T. R., Verreault, A., Luisi, B. F., and Laue, E. D. (2008). Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16, 1077-1085.
72. Muthuswamy, S., and Meier, I. (2011). Genetic and environmental changes in SUMO homeostasis lead to nuclear mRNA retention in plants. Planta 233, 201-208.
73. Nacerddine, K., Lehembre, F., Bhaumik, M., Artus, J., Cohen-Tannoudji, M., Babinet, C., Pandolfi, P. P., and Dejean, A. (2005). The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9, 769-779.
74. Nie, M., Xie, Y., Loo, J. A., and Courey, A. J. (2009). Genetic and proteomic evidence for roles of Drosophila SUMO in cell cycle control, Ras signaling, and early pattern formation. PLoS ONE 4, e5905. doi:10.1371/journal.pone.0005905
75. Novatchkova, M., Tomanov, K., Hofmann, K., Stuible, H. P., and Bachmair, A. (2012). Update on sumoylation: defining core components of the plant SUMO conjugation system by phylogenetic comparison. New Phytol. 195, 23-31.
76. Panse, V. G., Hardeland, U., Werner, T., Kuster, B., and Hurt, E. (2004). A proteome-wide approach identifies sumoylated substrate proteins in yeast. J. Biol. Chem. 279, 41346-41351.
77. Park, H. C., Choi, W., Park, H. J., Cheong, M. S., Koo, Y. D., Shin, G., Chung, W. S., Kim, W. Y., Kim, M. G., Bressan, R. A., Bohnert, H. J., Lee, S. Y., and Yun, D. J. (2011a). Identification and molecular properties of SUMO-binding proteins in Arabidopsis. Mol. Cells 32, 143-151.
78. Park, H. J., Kim, W. Y., Park, H. C., Lee, S. Y., Bohnert, H. J., and Yun, D. J. (2011b). SUMO and SUMOylation in plants. Mol. Cells 32, 305-316.
79. Pedrioli, P. G., Raught, B., Zhang, X. D., Rogers, R., Aitchison, J., Matunis, M., and Aebersold, R. (2006). Automated identification of SUMOylation sites using mass spectrometry and SUMmOn pattern recognition software. Nat. Methods 3, 533-539.
80. Perry, J. J., Tainer, J. A., and Boddy, M. N. (2008). A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem. Sci. 33, 201-208.
81. Saitoh, H., and Hinchey, J. (2000). Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J. Biol. Chem. 275, 6252-6258.
82. Samara, N. L., and Wolberger, C. (2011). A new chapter in the transcription SAGA. Curr. Opin. Struct. Biol. 21, 767-774.
83. Saracco, S. A., Miller, M. J., Kurepa, J., and Vierstra, R. D. (2007). Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol. 145, 119-134.
84. Schimmel, J., Larsen, K. M., Matic, I., Van Hagen, M., Cox, J., Mann, M., Andersen, J. S., and Vertegaal, A. C. O. (2008). The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol. Cell. Proteomics 7, 2107-2122.
85. Servet, C., Conde E Silva, N., and Zhou, D. X. (2010). Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol. Plant 3, 670-677.
86. Song, C. P., Agarwal, M., Ohta, M., Guo, Y., Halfter, U., Wang, P., and Zhu, J. K. (2005). Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384-2396.
87. Song, C. P., and Galbraith, D. W. (2006). AtSAP18, an orthologue of human SAP18, is involved in the regulation of salt stress and mediates transcriptional repression in Arabidopsis. Plant Mol. Biol. 60, 241-257.
88. Sridhar, V. V., Surendrarao, A., Gonzalez, D., Conlan, R. S., and Liu, Z. (2004). Transcriptional repression of target genes by LEUNIG and SEUSS, two interacting regulatory proteins for Arabidopsis flower development. Proc. Natl. Acad. Sci. U.S.A. 101, 11494-11499.
89. Srilunchang, K. O., Krohn, N. G., and Dresselhaus, T. (2010). DiSUMO-like DSUL is required for nuclei positioning, cell specification and viability during female gametophyte maturation in maize. Development 137, 333-345.
90. Sterner, D. E., Nathan, D., Reindle, A., Johnson, E. S., and Berger, S. L. (2006). Sumoylation of the yeast Gcn5 protein. Biochemistry 45, 1035-1042.
91. Stielow, B., Kruger, I., Diezko, R., Finkernagel, F., Gillemans, N., Kong-a-San, J., Philipsen, S., and Suske, G. (2010). Epigenetic silencing of spermatocyte-specific and neuronal genes by SUMO modification of the transcription factor Sp3. PLoS Genet. 6, e1001203. doi:10.1371/journal.pgen.1001203
92. Stielow, B., Sapetschnig, A., Kruger, I., Kunert, N., Brehm, A., Boutros, M., and Suske, G. (2008a). Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol. Cell 29, 742-754.
93. Stielow, B., Sapetschnig, A., Wink, C., Kruger, I., and Suske, G. (2008b). SUMO-modified Sp3 represses transcription by provoking local heterochromatic gene silencing. EMBO Rep. 9, 899-906.
94. Tatham, M. H., Matic, I., Mann, M., and Hay, R. T. (2011). Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci. Signal. 4, rs4.
95. Ullmann, R., Chien, C. D., Avantaggiati, M. L., and Muller, S. (2012). An acetylation switch regulates SUMO-dependent protein interaction networks. Mol. Cell 46, 759-770.
96. van den Burg, H. A., Kini, R. K., Schuurink, R. C., and Takken, F. L. W. (2010). Arabidopsis small ubiquitin-like modifier paralogs have distinct functions in development and defense. Plant Cell 22, 1998-2016.
97. Vassileva, M. T., and Matunis, M. J. (2004). SUMO modification of heterogeneous nuclear ribonucleoproteins. Mol. Cell. Biol. 24, 3623-3632.
98. Vertegaal, A. C. O. (2011). Uncovering ubiquitin and ubiquitin-like signaling networks. Chem. Rev. 111, 7923-7940.
99. Vertegaal, A. C. O., Andersen, J. S., Ogg, S. C., Hay, R. T., Mann, M., and Lamond, A. I. (2006). Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol. Cell. Proteomics 5, 2298-2310.
100. Vertegaal, A. C. O., Ogg, S. C., Jaffray, E., Rodriguez, M. S., Hay, R. T., Andersen, J. S., Mann, M., and Lamond, A. I. (2004). A proteomic study of SUMO-2 target proteins. J. Biol. Chem. 279, 33791-33798.
101. Vethantham, V., and Manley, J. L. (2009). "Emerging roles for SUMO in mRNA processing and metabolsim, " inSUMO regulation of cellular processes, ed. V. G. Wilson (Dordrecht: Springer), 41-57.
102. Wagner, S. A., Beli, P., Weinert, B. T., Nielsen, M. L., Cox, J., Mann, M., and Choudhary, C. (2011). A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol. Cell. Proteomics 10, M111 013284.
103. Wang, Y., Zhang, H., Chen, Y., Sun, Y., Yang, F., Yu, W., Liang, J., Sun, L., Yang, X., Shi, L., Li, R., Li, Y., Zhang, Y., Li, Q., Yi, X., and Shang, Y. (2009). LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660-672.
104. Westman, B. J., Verheggen, C., Hutten, S., Lam, Y. W., Bertrand, E., and Lamond, A. I. (2010). A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol. Cell 39, 618-631.
105. Wilkinson, K. A., and Henley, J. M. (2010). Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J. 428, 133-145.
106. Wohlschlegel, J. A., Johnson, E. S., Reed, S. I., and Yates, J. R. III. (2006). Improved identification of SUMO attachment sites using C-terminal SUMO mutants and tailored protease digestion strategies. J. Proteome Res. 5, 761-770.
107. Wohlschlegel, J. A., Johnson, E. S., Reed, S. I., and Yates, J. R. III. (2004). Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279, 45662-45668.
108. Wykoff, D. D., and O'shea, E. K. (2005). Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol. Cell. Proteomics 4, 73-83.
109. Xu, G., and Jaffrey, S. R. (2011). The new landscape of protein ubiquitination. Nat. Biotechnol. 29, 1098-1100.
110. Xu, G., Paige, J. S., and Jaffrey, S. R. (2010). Global analysis of lysine ubiquitination by ubiquitin remnant immunoaffinity profiling. Nat. Biotechnol. 28, 868-873.
111. Xu, X. M., Rose, A., Muthuswamy, S., Jeong, S. Y., Venkatakrishnan, S., Zhao, Q., and Meier, I. (2007). Nuclear pore anchor, the Arabidopsis homolog of Tpr/Mlp1/Mlp2/megator, is involved in mRNA export and SUMO homeostasis and affects diverse aspects of plant development. Plant Cell 19, 1537-1548.
112. Yost, H. J., and Lindquist, S. (1986). RNA splicing is interrupted by heat shock and is rescued by heat shock protein synthesis. Cell 45, 185-193.
113. Yu, C. W., Liu, X., Luo, M., Chen, C., Lin, X., Tian, G., Lu, Q., Cui, Y., and Wu, K. (2011). Histone deacetylase6 interacts with flowering LOCUS D and regulates flowering in Arabidopsis. Plant Physiol. 156, 173-184.
114. Zhang, H., Bishop, B., Ringenberg, W., Muir, W. M., and Ogas, J. (2012). The CHD3 remodeler pickle associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol. 159, 418-432.
115. Zhu, S., Goeres, J., Sixt, K. M., Bekes, M., Zhang, X. D., Salvesen, G. S., and Matunis, M. J. (2009). Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1. Mol. Cell 33, 570-580.