Abstract
Reversible post-translational modification is a rapid and efficient system to control the activity of pre-existing proteins. Modifiers range from small chemical moieties, such as phosphate groups, to proteins themselves as the modifier. The patriarch of the protein modifiers is ubiquitin which plays a central role in protein degradation and protein targeting. Over the last 20 years, the ubiquitin family has expanded to include a variety of ubiquitin-related small modifier proteins that are all covalently attached to a lysine residue on target proteins via series of enzymatic reactions. Of these more recently discovered ubiquitin-like proteins, the SUMO family has gained prominence as a major regulatory component that impacts numerous aspects of cell growth, differentiation, and response to stress. Unlike ubiquitinylation which often leads to proteins turn over, sumoylation performs a variety of function such as altering protein stability, modulating protein trafficking, directing protein-protein interactions, and regulating protein activity. This chapter will introduce the basic properties of SUMO proteins and the general tenets of sumoylation.
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Ayaydin F, Dasso M (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 15:5208–5218
Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, Jaenicke R, Becker J (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 280:275–286
Boddy MN, Howe K, Etkin LD, Solomon E, Freemont PS (1996) PIC 1, a novel ubiquitin-like protein which interacts with the PML component of a multiprotein complex that is disrupted in acute promyelocytic leukaemia. Oncogene 13:971–982
Bohren KM, Nadkarni V, Song JH, Gabbay KH, Owerbach D (2004) A M55 V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 279:27233–27238
Bueno MT, Richard S (2013) SUMOylation negatively modulates target gene occupancy of the KDM5B, a histone lysine demethylase. Epigenetics 8:1162–1175
Castro PH, Tavares RM, Bejarano ER, Azevedo H (2012) SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Sci 69:3269–3283
Chang CC, Naik MT, Huang YS, Jeng JC, Liao PH, Kuo HY, Ho CC, Hsieh YL, Lin CH, Huang NJ, Naik NM, Kung CCH, Lin SY, Chen RH, Chang KS, Huang TH, Shih HM (2011) Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol Cell 42:62–74
Chen A, Mannen H, Li SS (1998) Characterization of mouse ubiquitin-like SMT3A and SMT3B cDNAs and gene/pseudogenes. Biochem Mol Biol Int 46:1161–1174
Chung TL, Hsiao HH, Yeh YY, Shia HL, Chen YL, Liang PH, Wang AHJ, Khoo KH, Li SSL (2004) In vitro modification of human centromere protein CENP-C fragments by small ubiquitin-like modifier (SUMO) protein – definitive identification of the modification sites by tandem mass spectrometry analysis of the isopeptides. J Biol Chem 279:39653–39662
Chymkowitch P, Nguea AP, Aanes H, Koehler CJ, Thiede B, Lorenz S, Meza-Zepeda LA, Klungland A, Enserink JM (2015) Sumoylation of Rap1 mediates the recruitment of TFIID to promote transcription of ribosomal protein genes. Genome Res 25:897–906
Citro S, Chiocca S (2013) SUMO paralogs: redundancy and divergencies. Front Biosci 5:544–553
Cubenas-Potts C, Matunis MJ (2013) SUMO: a multifaceted modifier of chromatin structure and function. Dev Cell 24:1–12
de la Vega L, Grishina I, Moreno R, Kruger M, Braun T, Schmitz ML (2012) A redox-regulated SUMO/acetylation switch of HIPK2 controls the survival threshold to oxidative stress. Mol Cell 46:472–483
Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434
Desterro JM, Rodriguez MS, Hay RT (1998) SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol Cell 2:233–239
Deyrieux AF, Rosas-Acosta G, Ozbun MA, Wilson VG (2007) Sumoylation dynamics during keratinocyte differentiation. J Cell Sci 120:125–136
Dhall A, Wei S, Fierz B, Woodcock CL, Lee TH, Chatterjee C (2014) Sumoylated human histone H4 prevents chromatin compaction by inhibiting long-range internucleosomal interactions. J Biol Chem 289:33827–33837
Di Bacco A, Ouyang J, Lee HY, Catic A, Ploegh H, Gill G (2006) The SUMO-specific protease SENP5 is required for cell division. Mol Cell Biol 26:4489–4498
Ding HS, Xu YQ, Chen Q, Dai HM, Tang YJ, Wu JH, Shi YY (2005) Solution structure of human SUMO-3 C47S and its binding surface for Ubc9. Biochemist 44:2790–2799
Drag M, Mikolajczyk J, Krishnakumar IM, Huang ZW, Salvesen GS (2008) Activity profiling of human deSUMOylating enzymes (SENPs) with synthetic substrates suggests an unexpected specificity of two newly characterized members of the family. Biochem J 409:461–469
Eifler K, Vertegaal AC (2015) Mapping the SUMOylated landscape. FEBS J 282:3669–3680
Eladad S, Ye TZ, Hu P, Leversha M, Beresten S, Matunis MJ, Ellis NA (2005) Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum Mol Genet 14:1351–1365
Erker Y, Neyret-Kahn H, Seeler JS, Dejean A, Atfi A, Levy L (2013) Arkadia, a novel SUMO-targeted ubiquitin ligase involved in PML degradation. Mol Cell Biol 33:2163–2177
Escobar-Ramirez A, Vercoutter-Edouart AS, Mortuaire M, Huvent I, Hardiville S, Hoedt E, Lefebvre T, Pierce A (2015) Modification by SUMOylation controls both the transcriptional activity and the stability of delta-lactoferrin. PLoS One 10:e0129965
Evdokimov E, Sharma P, Lockett SJ, Lualdi M, Kuehn MR (2008) Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J Cell Sci 121:4106–4113
Garcia-Dominguez M, Reyes JC (2009) SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 1789:451–459
Gareau JR, Lima CD (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11:861–871
Gill G (2005) Something about SUMO inhibits transcription. Curr Opin Genet Dev 15:536–541
Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, Snowden AW, Garcia-Wilson E, Perkins ND, Hay RT (2003) p300 transcriptional repression is mediated by SUMO modification. Mol Cell 11:1043–1054
Gong L, Yeh ETH (2006) Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J Biol Chem 281:15869–15877
Gong LM, Millas S, Maul GG, Yeh ETH (2000) Differential regulation of sentrinized proteins by a novel sentrin-specific protease. J Biol Chem 275:3355–3359
Gonzalez-Prieto R, Cuijpers SA, Kumar R, Hendriks IA, Vertegaal AC (2015) c-Myc is targeted to the proteasome for degradation in a SUMOylation-dependent manner, regulated by PIAS1, SENP7 and RNF4. Cell Cycle 14:1859–1872
Goodson ML, Hong Y, Rogers R, Matunis MJ, Park-Sarge OK, Sarge KD (2001) SUMO-1 modification regulates the DNA binding activity of heat shock transcription factor 2, a promyelocytic leukemia nuclear body associated transcription factor. J Biol Chem 276:18513–18518
Hang J, Dasso M (2002) Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem 277:19961–19966
Hay RT (2005) SUMO: a history of modification. Mol Cell 18:1–12
Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I (2006) Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281:16117–16127
Hendriks IA, D’Souza RC, Yang B, Verlaan-de Vries M, Mann M, Vertegaal AC (2014) Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21:927–936
Hendriks IA, D’Souza RC, Chang JG, Mann M, Vertegaal AC (2015a) System-wide identification of wild-type SUMO-2 conjugation sites. Nat Commun 6:7289
Hendriks IA, Treffers LW, Verlaan-de Vries M, Olsen JV, Vertegaal AC (2015b) SUMO-2 orchestrates chromatin modifiers in response to DNA damage. Cell Rep 10:1778–1791
Hietakangas V, Anckar J, Blomster HA, Fujimoto M, Palvimo JJ, Nakai A, Sistonen L (2006) PDSM, a motif for phosphorylation-dependent SUMO modification. Proc Natl Acad Sci USA 103:45–50
Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141
Hong YL, Rogers R, Matunis MJ, Mayhew CN, Goodson M, Park-Sarge OK, Sarge KD (2001) Regulation of heat shock transcription factor 1 by stress-induced SUMO-1 modification. J Biol Chem 276:40263–40267
Huang WC, Ko TP, Li SSL, Wang AHJ (2004) Crystal structures of the human SUMO-2 protein at 1.6 angstrom and 1.2 angstrom resolution – implication on the functional differences of SUMO proteins. Eur J Biochem 271:4114–4122
Huang C, Cheng J, Bawa-Khalfe T, Yao X, Chin YE, Yeh ET (2016) SUMOylated ORC2 recruits a histone demethylase to regulate centromeric histone modification and genomic stability. Cell Rep 15:147–157
Ihara M, Koyama H, Uchimura Y, Saitoh H, Kikuchi A (2007) Noncovalent binding of small ubiquitin-related modifier (SUMO) protease to SUMO is necessary for enzymatic activities and cell growth. J Biol Chem 282:16465–16475
Jentsch S, Psakhye I (2013) Control of nuclear activities by substrate-selective and protein-group SUMOylation. Annu Rev Genet 47:167–186
Johnson ES, Gupta AA (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735–744
Johnson ES, Schwienhorst I, Dohmen RJ, Blobel G (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J 16:5509–5519
Jones D, Crowe E, Stevens TA, Candido EP (2002) Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol 3:0002.1–0002.15
Kagey MH, Melhuish TA, Wotton D (2003) The polycomb protein Pc2 is a SUMO E3. Cell 113:127–137
Kamitani T, Kito K, Nguyen HP, Fukuda-Kamitani T, Yeh ET (1998a) Characterization of a second member of the sentrin family of ubiquitin-like proteins. J Biol Chem 273:11349–11353
Kamitani T, Kito K, Nguyen HP, Wada H, Fukuda-Kamitani T, Yeh ET (1998b) Identification of three major sentrinization sites in PML. J Biol Chem 273:26675–26682
Kim YH, Choi CY, Kim Y (1999) Covalent modification of the homeodomain-interacting protein kinase 2 (HIPK2) by the ubiquitin-like protein SUMO-1. Proc Natl Acad Sci U S A 96:12350–12355
Klenk C, Humrich J, Quitterer U, Lohse MJ (2006) SUMO-1 controls the protein stability and the biological function of phosducin. J Biol Chem 281:8357–8364
Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (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
Lee B, Muller MT (2009) SUMOylation enhances DNA methyltransferase 1 activity. Biochem J 421:449–461
Lehembre F, Badenhorst P, Muller S, Travers A, Schweisguth F, Dejean A (2000) Covalent modification of the transcriptional repressor tramtrack by the ubiquitin-related protein Smt3 in Drosophila flies. Mol Cell Biol 20:1072–1082
Lewicki MC, Srikumar T, Johnson E, Raught B (2015) The S. cerevisiae SUMO stress response is a conjugation-deconjugation cycle that targets the transcription machinery. J Proteomics 118:39–48
Li SJ, Hochstrasser M (1999) A new protease required for cell-cycle progression in yeast. Nature 398:246–251
Lima CD, Reverter D (2008) Structure of the human SENP7 catalytic domain and poly-SUMO deconjugation activities for SENP6 and SENP7. J Biol Chem 283:32045–32055
Lois LM, Lima CD (2005) Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J 24:439–451
Long JY, Wang GN, He DM, Liu F (2004) Repression of Smad4 transcriptional activity by SUMO modification. Biochem J 379:23–29
Manza LL, Codreanu SG, Stamer SL, Smith DL, Wells KS, Roberts RL, Liebler DC (2004) Global shifts in protein sumoylation in response to electrophile and oxidative stress. Chem Res Toxicol 17:1706–1715
Matic I, Macek B, Hilger M, Walther TC, Mann M (2008) Phosphorylation of SUMO-1 occurs in vivo and is conserved through evolution. J Proteome Res 7:4050–4057
Matic I, Schimmel J, Hendriks IA, van Santen MA, van de Rijke F, van Dam H, Gnad F, Mann M, Vertegaal ACO (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
Matunis MJ, Coutavas E, Blobel G (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol 135:1457–1470
Melchior F (2000) SUMO – nonclassical ubiquitin. Annu Rev Cell Dev Biol 16:591–626
Meulmeester E, Kunze M, Hsiao HH, Urlaub H, Melchior F (2008) Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol Cell 30:610–619
Mikolajczyk J, Drag M, Bekes M, Cao JT, Ronai Z, Salvesen GS (2007) Small ubiquitin-related modifier (SUMO)-specific proteases – profiling the specificities and activities of human SENPs. J Biol Chem 282:26217–26224
Namanja AT, Li YJ, Su Y, Wong S, Lu J, Colson LT, Wu C, Li SS, Chen Y (2012) Insights into high affinity small ubiquitin-like modifier (SUMO) recognition by SUMO-interacting motifs (SIMs) revealed by a combination of NMR and peptide array analysis. J Biol Chem 287:3231–3240
Nathan D, Ingvarsdottir K, Sterner DE, Bylebyl GR, Dokmanovic M, Dorsey LA, Whelan KA, Krsmanovic M, Lane WS, Meluh PB, Johnson ES, Berger SL (2006) Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev 20:966–976
Nayak A, Muller S (2014) SUMO-specific proteases/isopeptidases: SENPs and beyond. Genome Biol 15:422
Okura T, Gong L, Kamitani T, Wada T, Okura I, Wei CF, Chang HM, Yeh ET (1996) Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J Immunol 157:4277–4281
Owerbach D, McKay EM, Yeh ET, Gabbay KH, Bohren KM (2005) A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem Biophys Res Commun 337:517–520
Perry JJP, Tainer JA, Boddy MN (2008) A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 33:201–208
Picard N, Caron V, Bilodeau S, Sanchez M, Mascle X, Aubry M, Tremblay A (2012) Identification of estrogen receptor beta as a SUMO-1 target reveals a novel phosphorylated sumoylation motif and regulation by glycogen synthase kinase 3beta. Mol Cell Biol 32:2709–2721
Pichler A, Gast A, Seeler JS, Dejean A, Melchior F (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109–120
Potts PR, Yu HT (2005) Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol Cell Biol 25:7021–7032
Prudden J, Pebernard S, Raffa G, Slavin DA, Perry JJP, Tainer JA, McGowan CH, Boddy MN (2007) SUMO-targeted ubiquitin ligases in genome stability. EMBO J 26:4089–4101
Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151:807–820
Raman N, Nayak A, Muller S (2013) The SUMO system: a master organizer of nuclear protein assemblies. Chromosoma 122:475–485
Rangasamy D, Woytek K, Khan SA, Wilson VG (2000) SUMO-1 modification of bovine papillomavirus E1 protein is required for intranuclear accumulation. J Biol Chem 275:37999–38004
Riising EM, Boggio R, Chiocca S, Helin K, Pasini D (2008) The polycomb repressive complex 2 is a potential target of SUMO modifications. PLoS One 3:e2704
Rosas-Acosta G, Russell WK, Deyrieux A, Russell DH, Wilson VG (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol Cell Proteomics 4:56–72
Ross S, Best JL, Zon LI, Gill G (2002) SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol Cell 10:831–842
Rytinki MM, Kaikkonen S, Pehkonen P, Jaaskelainen T, Palvimo JJ (2009) PIAS proteins: pleiotropic interactors associated with SUMO. Cell Mol Life Sci 66:3029–3041
Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15:3088–3103
Sahin U, de The H, Lallemand-Breitenbach V (2014) PML nuclear bodies: assembly and oxidative stress-sensitive sumoylation. Nucleus 5:499–507
Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275:6252–6258
Schmidt D, Muller S (2002) Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc Natl Acad Sci U S A 99:2872–2877
Sekiyama N, Ikegami T, Yamane T, Ikeguchi M, Uchimura Y, Baba D, Ariyoshi M, Tochio H, Saitoh H, Shirakawa M (2008) Structure of the small ubiquitin-like modifier (SUMO)-interacting motif of MBD1-containing chromatin-associated factor 1 bound to SUMO-3. J Biol Chem 283:35966–35975
Sharma P, Yamada S, Lualdi M, Dasso M, Kuehn MR (2013) SENP1 is essential for desumoylating SUMO1-modified proteins but dispensable for SUMO2 and SUMO3 deconjugation in the mouse embryo. Cell Rep 3:1640–1650
Sharrocks AD (2006) PIAS proteins and transcriptional regulation – more than just SUMO E3 ligases? Genes Dev 20:754–758
Shen ZY, Pardingtonpurtymun PE, Comeaux JC, Moyzis RK, Chen DJ (1996) Ubl1, a human ubiquitin-like protein associating with human rad51/rad52 proteins. Genomics 36:271–279
Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci U S A 100:13225–13230
Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen YA (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci U S A 101:14373–14378
Spektor TM, Congdon LM, Veerappan CS, Rice JC (2011) The UBC9 E2 SUMO conjugating enzyme binds the PR-Set7 histone methyltransferase to facilitate target gene repression. PLoS One 6:e22785
Sun H, Leverson JD, Hunter T (2007) Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J 26:4102–4112
Tammsalu T, Matic I, Jaffray EG, Ibrahim AF, Tatham MH, Hay RT (2015) Proteome-wide identification of SUMO modification sites by mass spectrometry. Nat Protoc 10:1374–1388
Tatemichi Y, Shibazaki M, Yasuhira S, Kasai S, Tada H, Oikawa H, Suzuki Y, Takikawa Y, Masuda T, Maesawa C (2015) Nucleus accumbens associated 1 is recruited within the promyelocytic leukemia nuclear body through SUMO modification. Cancer Sci 106:848–856
Tatham MH, Jaffray E, Vaughan OA, Desterro JMP, Botting CH, Naismith JH, Hay RT (2001) Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 276:35368–35374
Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10:538–546
Tempe D, Piechaczyk M, Bossis G (2008) SUMO under stress. Biochem Soc Trans 36:874–878
Tong H, Hateboer G, Perrakis A, Bernards R, Sixma TK (1997) Crystal structure of murine/human Ubc9 provides insight into the variability of the ubiquitin-conjugating system. J Biol Chem 272:21381–21387
Ungureanu D, Vanhatupa S, Kotaja N, Yang J, Aittomaki S, Janne OA, Palvimo JJ, Silvennoinen O (2003) PIAS proteins promote SUMO-1 conjugation to STAT1. Blood 102:3311–3313
Uzunova K, Gottsche K, Miteva M, Weisshaar SR, Glanemann C, Schnellhardt M, Niessen M, Scheel H, Hofmann K, Johnson ES, Praefcke GJ, Dohmen RJ (2007) Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282:34167–34175
Van Nguyen T, Angkasekwinai P, Dou H, Lin FM, Lu LS, Cheng J, Chin YE, Dong C, Yeh ET (2012) SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Mol Cell 45:210–221
Verger A, Perdomo J, Crossley M (2003) Modification with SUMO – a role in transcriptional regulation. EMBO Rep 4:137–142
Vertegaal ACO, Andersen JS, Ogg SC, Hay RT, Mann M, Lamond AI (2006) Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics. Mol Cell Proteomics 5:2298–2310
Wagner T, Kiweler N, Wolff K, Knauer SK, Brandl A, Hemmerich P, Dannenberg JH, Heinzel T, Schneider G, Kramer OH (2015) Sumoylation of HDAC2 promotes NF-kappaB-dependent gene expression. Oncotarget 6:7123–7135
Wang J, Taherbhoy AM, Hunt HW, Seyedin SN, Miller DW, Miller DJ, Huang DT, Schulman BA (2010) Crystal Structure of UBA2(ufd)-Ubc9: insights into E1-E2 interactions in SUMO pathways. PLoS One 5:e15805
Wang L, Wansleeben C, Zhao S, Miao P, Paschen W, Yang W (2014) SUMO2 is essential while SUMO3 is dispensable for mouse embryonic development. EMBO Rep 15:878–885
Wasik U, Filipek A (2014) Non-nuclear function of sumoylated proteins. Biochim Biophys Acta 1843:2878–2885
Weger S, Hammer E, Heilbronn R (2005) Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett 579:5007–5012
Wei F, Scholer HR, Atchison ML (2007) Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem 282:21551–21560
Wei WZ, Yang P, Pang JF, Zhang S, Wang Y, Wang MH, Dong Z, She JX, Wang CY (2008) A stress-dependent SUMO4 sumoylation of its substrate proteins. Biochem Biophys Res Commun 375:454–459
Wilson VG (2004) Sumoylation: molecular biology and biochemistry. Horizon Biosciences, Norfolk
Wu YC, Bian XL, Heaton PH, Deyrieux AF, Wilson VG (2009) Host cell sumoylation level influences papillomavirus E2 protein stability. Virology 387:176–183
Xiao Z, Chang JG, Hendriks IA, Sigurethsson JO, Olsen JV, Vertegaal AC (2015) System-wide analysis of SUMOylation dynamics in response to replication stress reveals novel small ubiquitin-like modified target proteins and acceptor lysines relevant for genome stability. Mol Cell Proteomics 14:1419–1434
Xie Y, Kerscher O, Kroetz MB, McConchie HF, Sung P, Hochstrasser M (2007) The yeast HEX3-SLX8 heterodimer is a ubiquitin ligase stimulated by substrate sumoylation. J Biol Chem 282:34176–34184
Yang W, Paschen W (2015) SUMO proteomics to decipher the SUMO-modified proteome regulated by various diseases. Proteomics 15:1181–1191
Yang SH, Jaffray E, Hay RT, Sharrocks AD (2003) Dynamic interplay of the SUMO and ERK pathways in regulating Elk-1 transcriptional activity. Mol Cell 12:63–74
Yang ML, Hsu CT, Ting CY, Liu LF, Hwang JL (2006a) Assembly of a polymeric chain of SUMO1 on human topoisomerase I in vitro. J Biol Chem 281:8264–8274
Yang SH, Galanis A, Witty J, Sharrocks AD (2006b) An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J 25:5083–5093
Zhang FP, Mikkonen L, Toppari J, Palvimo JJ, Thesleff I, Janne OA (2008) SUMO-1 function is dispensable in normal mouse development. Mol Cell Biol 28:5381–5390
Zheng J, Liu L, Wang S, Huang X (2015) SUMO-1 promotes Ishikawa cell proliferation and apoptosis in endometrial cancer by increasing Sumoylation of histone H4. Int J Gynecol Cancer 25:1364–1368
Zhou W, Ryan JJ, Zhou H (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae – induction of protein sumoylation by cellular stresses. J Biol Chem 279:32262–32268
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We wish to thank other current and former members of the Wilson lab for discussions that helped form much of the work presented here.
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Wilson, V.G. (2017). Introduction to Sumoylation. In: Wilson, V. (eds) SUMO Regulation of Cellular Processes. Advances in Experimental Medicine and Biology, vol 963. Springer, Cham. https://doi.org/10.1007/978-3-319-50044-7_1
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