Multiple crosstalks between mRNA biogenesis and SUMO
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Abstract
mRNA metabolism involves the orchestration of multiple nuclear events, including transcription, processing (e.g., capping, splicing, polyadenylation), and quality control. This leads to the accurate formation of messenger ribonucleoparticles (mRNPs) that are finally exported to the cytoplasm for translation. The production of defined sets of mRNAs in given environmental or physiological situations relies on multiple regulatory mechanisms that target the mRNA biogenesis machineries. Among other regulations, post-translational modification by the small ubiquitin-like modifier SUMO, whose prominence in several cellular processes has been largely demonstrated, also plays a key role in mRNA biogenesis. Analysis of the multiple available SUMO proteomes and functional validations of an increasing number of sumoylated targets have revealed the key contribution of SUMO-dependent regulation in nuclear mRNA metabolism. While sumoylation of transcriptional activators and repressors is so far best documented, SUMO contribution to other stages of mRNA biogenesis is also emerging. Modification of mRNA metabolism factors by SUMO determine their subnuclear targeting and biological activity, notably by regulating their molecular interactions with nucleic acids or protein partners. In particular, sumoylation of DNA-bound transcriptional regulators interfere with their association to target sequences or chromatin modifiers. In addition, the recent identification of enzymes of the SUMO pathway within specialized mRNA biogenesis machineries may provide a further level of regulation to their specificity. These multiple crosstalks between mRNA metabolism and SUMO appear therefore as important players in cellular regulatory networks.
Keywords
Sumoylation mRNA transcription mRNA processing Messenger ribonucleoparticle (mRNP)Abbreviations
- hnRNP
Heterogenous nuclear ribonucleoprotein
- mRNA
Messenger RNA
- mRNP
Messenger ribonucleoparticle
- NPC
Nuclear pore complex
- RNAP II
RNA polymerase II
- SIM
SUMO-interacting motif
- STUbL
SUMO-targeted ubiquitin ligase
- SUMO
Small ubiquitin-like modifier
Notes
Acknowledgments
We thank Amandine Bonnet, Valérie Doye, Anne-Lise Haenni, and Françoise Stutz for critical reading of the manuscript and apologize to colleagues whose work was not directly cited due to space limitation. Our research is supported by the CNRS, the Fondation ARC pour la Recherche sur le Cancer (Grant “Projet ARC”, to B.P.) and La Ligue Contre le Cancer (comité du Val d'Oise, to B.P.). J.O.R is the recipient of a PhD fellowship from the Ministère de l'Enseignement Supérieur et de la Recherche.
References
- Abed M, Barry KC, Kenyagin D, Koltun B, Phippen TM, Delrow JJ, Parkhurst SM, Orian A (2011) Degringolade, a SUMO-targeted ubiquitin ligase, inhibits Hairy/Groucho-mediated repression. EMBO J 30(7):1289–1301PubMedCrossRefGoogle Scholar
- Anckar J, Hietakangas V, Denessiouk K, Thiele DJ, Johnson MS, Sistonen L (2006) Inhibition of DNA binding by differential sumoylation of heat shock factors. Mol Cell Biol 26(3):955–964PubMedCrossRefGoogle Scholar
- Babic I, Cherry E, Fujita DJ (2006) SUMO modification of Sam68 enhances its ability to repress cyclin D1 expression and inhibits its ability to induce apoptosis. Oncogene 25(36):4955–4964PubMedCrossRefGoogle Scholar
- Babour A, Dargemont C, Stutz F (2012) Ubiquitin and assembly of export competent mRNP. Biochim Biophys Acta 1819(6):521–530PubMedCrossRefGoogle Scholar
- Bernardi R, Pandolfi PP (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8(12):1006–1016PubMedCrossRefGoogle Scholar
- Blomster HA, Hietakangas V, Wu J, Kouvonen P, Hautaniemi S, Sistonen L (2009) Novel proteomics strategy brings insight into the prevalence of SUMO-2 target sites. Mol Cell Proteomics 8(6):1382–1390PubMedCrossRefGoogle Scholar
- Bouras T, Fu M, Sauve AA, Wang F, Quong AA, Perkins ND, Hay RT, Gu W, Pestell RG (2005) SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1. J Biol Chem 280(11):10264–10276PubMedCrossRefGoogle Scholar
- Bruderer R, Tatham MH, Plechanovova A, Matic I, Garg AK, Hay RT (2011) Purification and identification of endogenous polySUMO conjugates. EMBO Rep 12(2):142–148PubMedCrossRefGoogle Scholar
- Budhiraja R, Hermkes R, Muller S, Schmidt J, Colby T, Panigrahi K, Coupland G, 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(3):1529–1540PubMedCrossRefGoogle Scholar
- Chen X, Ding B, LeJeune D, Ruggiero C, Li S (2009) Rpb1 sumoylation in response to UV radiation or transcriptional impairment in yeast. PLoS One 4(4):e5267. doi: 10.1371/journal.pone.0005267 PubMedCrossRefGoogle Scholar
- del Olmo M, Mizrahi N, Gross S, Moore CL (1997) The Uba2 and Ufd1 proteins of Saccharomyces cerevisiae interact with poly(A) polymerase and affect the polyadenylation activity of cell extracts. Mol Gen Genet 255(2):209–218PubMedCrossRefGoogle Scholar
- Denison C, Rudner AD, Gerber SA, Bakalarski CE, Moazed D, Gygi SP (2005) A proteomic strategy for gaining insights into protein sumoylation in yeast. Mol Cell Proteomics 4(3):246–254PubMedCrossRefGoogle Scholar
- Desterro JM, Keegan LP, Jaffray E, Hay RT, O'Connell MA, Carmo-Fonseca M (2005) SUMO-1 modification alters ADAR1 editing activity. Mol Biol Cell 16(11):5115–5126PubMedCrossRefGoogle Scholar
- Dieppois G, Iglesias N, Stutz F (2006) Cotranscriptional recruitment to the mRNA export receptor Mex67p contributes to nuclear pore anchoring of activated genes. Mol Cell Biol 26(21):7858–7870PubMedCrossRefGoogle Scholar
- Elrouby N, 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(40):17415–17420PubMedCrossRefGoogle Scholar
- Fanis P, Gillemans N, Aghajanirefah A, Pourfarzad F, Demmers J, Esteghamat F, Vadlamudi RK, Grosveld F, Philipsen S, van Dijk TB (2012) Five Friends of Methylated Chtop, a complex linking arginine methylation to desumoylation. Mol Cell Proteomics 11(11):1263–1273. doi: 10.1074/mcp.M112.017194 PubMedCrossRefGoogle Scholar
- Finkbeiner E, Haindl M, Muller S (2011) The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J 30(6):1067–1078PubMedCrossRefGoogle Scholar
- Ganesan AK, Kho Y, Kim SC, Chen Y, Zhao Y, White MA (2007) Broad spectrum identification of SUMO substrates in melanoma cells. Proteomics 7(13):2216–2221. doi: 10.1002/pmic.200600971 PubMedCrossRefGoogle Scholar
- Garcia-Dominguez M, Reyes JC (2009) SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 1789(6–8):451–459PubMedGoogle Scholar
- Garcia-Gutierrez P, Juarez-Vicente F, Gallardo-Chamizo F, Charnay P, Garcia-Dominguez M (2011) The transcription factor Krox20 is an E3 ligase that sumoylates its Nab coregulators. EMBO Rep 12(10):1018–1023. doi: 10.1038/embor.2011.152 PubMedCrossRefGoogle Scholar
- Gareau JR, Lima CD (2010) The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat Rev Mol Cell Biol 11(12):861–871PubMedCrossRefGoogle Scholar
- Garee JP, Meyer R, Oesterreich S (2011) Co-repressor activity of scaffold attachment factor B1 requires sumoylation. Biochem Biophys Res Commun 408(4):516–522PubMedCrossRefGoogle Scholar
- Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8:947–956PubMedCrossRefGoogle Scholar
- Geoffroy MC, Hay RT (2009) An additional role for SUMO in ubiquitin-mediated proteolysis. Nat Rev Mol Cell Biol 10(8):564–568PubMedCrossRefGoogle Scholar
- Gill G (2005) Something about SUMO inhibits transcription. Curr Opin Genet Dev 15(5):536–541PubMedCrossRefGoogle Scholar
- 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(4):1043–1054PubMedCrossRefGoogle Scholar
- Girdwood DW, Tatham MH, Hay RT (2004) SUMO and transcriptional regulation. Semin Cell Dev Biol 15(2):201–210PubMedCrossRefGoogle Scholar
- Gocke CB, Yu H, Kang J (2005) Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates. J Biol Chem 280(6):5004–5012PubMedCrossRefGoogle Scholar
- Goeres J, Chan PK, Mukhopadhyay D, Zhang H, Raught B, Matunis MJ (2011) The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup107-160 nucleoporin subcomplex. Mol Biol Cell 22(24):4868–4882PubMedCrossRefGoogle Scholar
- Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, Cox J, Barton GJ, Mann M, Hay RT (2009) System-wide changes to SUMO modifications in response to heat shock. Sci Signal 2(72):ra24PubMedCrossRefGoogle Scholar
- Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, Del Sal G (1999) Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 18(22):6462–6471. doi: 10.1093/emboj/18.22.6462 PubMedCrossRefGoogle Scholar
- Green DM, Johnson CP, Hagan H, Corbett AH (2003) The C-terminal domain of myosin-like protein 1 (Mlp1p) is a docking site for heterogeneous nuclear ribonucleoproteins that are required for mRNA export. Proc Natl Acad Sci U S A 100(3):1010–1015PubMedCrossRefGoogle Scholar
- Hannich JT, Lewis A, Kroetz MB, Li SJ, Heide H, Emili A, Hochstrasser M (2005) Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J Biol Chem 280(6):4102–4110PubMedCrossRefGoogle Scholar
- Hickey CM, Wilson NR, Hochstrasser M (2012) Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 13(12):755–766. doi: 10.1038/nrm3478 PubMedCrossRefGoogle Scholar
- Holmstrom S, Van Antwerp ME, Iniguez-Lluhi JA (2003) Direct and distinguishable inhibitory roles for SUMO isoforms in the control of transcriptional synergy. Proc Natl Acad Sci U S A 100(26):15758–15763. doi: 10.1073/pnas.2136933100 PubMedCrossRefGoogle Scholar
- Ihara M, Stein P, Schultz RM (2008) UBE2I (UBC9), a SUMO-conjugating enzyme, localizes to nuclear speckles and stimulates transcription in mouse oocytes. Biol Reprod 79(5):906–913PubMedCrossRefGoogle Scholar
- 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(18):5509–5519. doi: 10.1093/emboj/16.18.5509 PubMedCrossRefGoogle Scholar
- Kashyap AK, Schieltz D, Yates J 3rd, Kellogg DR (2005) Biochemical and genetic characterization of Yra1p in budding yeast. Yeast 22(1):43–56PubMedCrossRefGoogle Scholar
- Lee SW, Lee MH, Park JH, Kang SH, Yoo HM, Ka SH, Oh YM, Jeon YJ, Chung CH (2012) SUMOylation of hnRNP-K is required for p53-mediated cell-cycle arrest in response to DNA damage. EMBO J. doi: 10.1038/emboj.2012.293 Google Scholar
- Li T, Evdokimov E, Shen RF, Chao CC, Tekle E, Wang T, Stadtman ER, Yang DC, Chock PB (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(23):8551–8556PubMedCrossRefGoogle Scholar
- Lin X, Sun B, Liang M, Liang YY, Gast A, Hildebrand J, Brunicardi FC, Melchior F, Feng XH (2003) Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol Cell 11(5):1389–1396PubMedCrossRefGoogle Scholar
- Liu B, Shuai K (2009) Summon SUMO to wrestle with inflammation. Mol Cell 35(6):731–732. doi: 10.1016/j.molcel.2009.09.002 PubMedCrossRefGoogle Scholar
- Lomeli H, Vazquez M (2011) Emerging roles of the SUMO pathway in development. Cell Mol Life Sci 68(24):4045–4064. doi: 10.1007/s00018-011-0792-5 PubMedCrossRefGoogle Scholar
- Long J, Zuo D, Park M (2005) Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J Biol Chem 280(42):35477–35489PubMedCrossRefGoogle Scholar
- Luna R, Gaillard H, Gonzalez-Aguilera C, Aguilera A (2008) Biogenesis of mRNPs: integrating different processes in the eukaryotic nucleus. Chromosoma 117(4):319–331. doi: 10.1007/s00412-008-0158-4 PubMedCrossRefGoogle Scholar
- Lyst MJ, Stancheva I (2007) A role for SUMO modification in transcriptional repression and activation. Biochem Soc Trans 35(Pt 6):1389–1392PubMedCrossRefGoogle Scholar
- Lyst MJ, Nan X, Stancheva I (2006) Regulation of MBD1-mediated transcriptional repression by SUMO and PIAS proteins. EMBO J 25(22):5317–5328PubMedCrossRefGoogle Scholar
- 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(12):1706–1715. doi: 10.1021/tx049767l PubMedCrossRefGoogle Scholar
- Meier I (2012) mRNA export and sumoylation-Lessons from plants. Biochim Biophys Acta 1819(6):531–537PubMedCrossRefGoogle Scholar
- Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD (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(38):16512–16517PubMedCrossRefGoogle Scholar
- Miller MJ, Scalf M, Rytz TC, Hubler SL, Smith LM, Vierstra RD (2012) Quantitative proteomics reveal factors regulating RNA biology as dynamics targets of stress-induced sumoylation in Arabidopsis. Mol Cell Proteomics 12(2):449–463. doi: 10.1074/mcp.M112.025056 PubMedGoogle Scholar
- Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20(4):223–232PubMedCrossRefGoogle Scholar
- Mullen JR, Chen CF, Brill SJ (2010) Wss1 is a SUMO-dependent isopeptidase that interacts genetically with the Slx5-Slx8 SUMO-targeted ubiquitin ligase. Mol Cell Biol 30(15):3737–3748PubMedCrossRefGoogle Scholar
- Muromoto R, Ishida M, Sugiyama K, Sekine Y, Oritani K, Shimoda K, Matsuda T (2006) Sumoylation of Daxx regulates IFN-induced growth suppression of B lymphocytes and the hormone receptor-mediated transactivation. J Immunol 177(2):1160–1170PubMedGoogle Scholar
- Nacerddine K, Lehembre F, Bhaumik M, Artus J, Cohen-Tannoudji M, Babinet C, Pandolfi PP, Dejean A (2005) The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 9(6):769–779PubMedCrossRefGoogle Scholar
- Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, Varela E, Hediger F, Gasser SM, Krogan NJ (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322(5901):597–602PubMedCrossRefGoogle Scholar
- Navascues J, Bengoechea R, Tapia O, Casafont I, Berciano MT, Lafarga M (2008) SUMO-1 transiently localizes to Cajal bodies in mammalian neurons. J Struct Biol 163(2):137–146PubMedCrossRefGoogle Scholar
- Oeffinger M, Zenklusen D (2012) To the pore and through the pore: a story of mRNA export kinetics. Biochim Biophys Acta 1819:494–506PubMedCrossRefGoogle Scholar
- Palancade B, Doye V (2008) Sumoylating and desumoylating enzymes at nuclear pores: underpinning their unexpected duties? Trends Cell Biol 18(4):174–183PubMedCrossRefGoogle Scholar
- Panse VG, Hardeland U, Werner T, Kuster B, Hurt E (2004) A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279(40):41346–41351. doi: 10.1074/jbc.M407950200 PubMedCrossRefGoogle Scholar
- Panse VG, Kressler D, Pauli A, Petfalski E, Gnadig M, Tollervey D, Hurt E (2006) Formation and nuclear export of preribosomes are functionally linked to the small-ubiquitin-related modifier pathway. Traffic 7(10):1311–1321PubMedCrossRefGoogle Scholar
- Pelisch F, Gerez J, Druker J, Schor IE, Munoz MJ, Risso G, Petrillo E, Westman BJ, Lamond AI, Arzt E, Srebrow A (2010) The serine/arginine-rich protein SF2/ASF regulates protein sumoylation. Proc Natl Acad Sci U S A 107(37):16119–16124PubMedCrossRefGoogle Scholar
- Pelisch F, Pozzi B, Risso G, Munoz MJ, Srebrow A (2012) DNA damage-induced heterogeneous nuclear ribonucleoprotein K sumoylation regulates p53 transcriptional activation. J Biol Chem 287(36):30789–30799. doi: 10.1074/jbc.M112.390120 PubMedCrossRefGoogle Scholar
- Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151(4):807–820PubMedCrossRefGoogle Scholar
- Pungaliya P, Kulkarni D, Park HJ, Marshall H, Zheng H, Lackland H, Saleem A, Rubin EH (2007) TOPORS functions as a SUMO-1 E3 ligase for chromatin-modifying proteins. J Proteome Res 6(10):3918–3923. doi: 10.1021/pr0703674 PubMedCrossRefGoogle Scholar
- Rappsilber J, Ryder U, Lamond AI, Mann M (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12(8):1231–1245. doi: 10.1101/gr.473902 PubMedCrossRefGoogle Scholar
- Rodriguez MS, Desterro JM, Lain S, Midgley CA, Lane DP, Hay RT (1999) SUMO-1 modification activates the transcriptional response of p53. EMBO J 18(22):6455–6461. doi: 10.1093/emboj/18.22.6455 PubMedCrossRefGoogle Scholar
- 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(1):56–72PubMedGoogle Scholar
- Rosonina E, Duncan SM, Manley JL (2010) SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev 24(12):1242–1252PubMedCrossRefGoogle Scholar
- Schimmel J, Larsen KM, Matic I, van Hagen M, Cox J, Mann M, Andersen JS, Vertegaal AC (2008) The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol Cell Proteomics 7:2107–2122PubMedCrossRefGoogle Scholar
- Schimmel J, Balog CI, Deelder AM, Drijfhout JW, Hensbergen PJ, Vertegaal AC (2010) Positively charged amino acids flanking a sumoylation consensus tetramer on the 110 kDa tri-snRNP component SART1 enhance sumoylation efficiency. J Proteomics 73(8):1523–1534PubMedCrossRefGoogle Scholar
- Schulz S, Chachami G, Kozaczkiewicz L, Winter U, Stankovic-Valentin N, Haas P, Hofmann K, Urlaub H, Ovaa H, Wittbrodt J, Meulmeester E, Melchior F (2012) Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep 13(10):930–938. doi: 10.1038/embor.2012.125 PubMedCrossRefGoogle Scholar
- Seeler JS, Dejean A (2003) Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 4(9):690–699. doi: 10.1038/nrm1200 PubMedCrossRefGoogle Scholar
- Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci U S A 100(23):13225–13230. doi: 10.1073/pnas.1735528100 PubMedCrossRefGoogle Scholar
- Stehmeier P, Muller S (2009) Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol Cell 33(3):400–409. doi: 10.1016/j.molcel.2009.01.013 PubMedCrossRefGoogle Scholar
- Sun H, Hunter T (2012) Poly-small ubiquitin-like modifier (PolySUMO)-binding proteins identified through a string search. J Biol Chem 287(50):42071–42083. doi: 10.1074/jbc.M112.410985 Google Scholar
- Tan-Wong SM, Wijayatilake HD, Proudfoot NJ (2009) Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23(22):2610–2624PubMedCrossRefGoogle Scholar
- Tateishi Y, Ariyoshi M, Igarashi R, Hara H, Mizuguchi K, Seto A, Nakai A, Kokubo T, Tochio H, Shirakawa M (2009) Molecular basis for SUMOylation-dependent regulation of DNA binding activity of heat shock factor 2. J Biol Chem 284(4):2435–2447PubMedCrossRefGoogle Scholar
- Tatham MH, Matic I, Mann M, Hay RT (2011) Comparative proteomic analysis identifies a role for SUMO in protein quality control. Sci Signal 4(178):rs4PubMedCrossRefGoogle Scholar
- Tutucci E, Stutz F (2011) Keeping mRNPs in check during assembly and nuclear export. Nat Rev Mol Cell Biol 12(6):377–384PubMedCrossRefGoogle Scholar
- Uchimura Y, Ichimura T, Uwada J, Tachibana T, Sugahara S, Nakao M, Saitoh H (2006) Involvement of SUMO modification in MBD1- and MCAF1-mediated heterochromatin formation. J Biol Chem 281(32):23180–23190PubMedCrossRefGoogle Scholar
- Ullmann R, Chien CD, Avantaggiati ML, Muller S (2012) An acetylation switch regulates SUMO-dependent protein interaction networks. Mol Cell 46(6):759–770. doi: 10.1016/j.molcel.2012.04.006 PubMedCrossRefGoogle Scholar
- Vassileva MT, Matunis MJ (2004) SUMO modification of heterogeneous nuclear ribonucleoproteins. Mol Cell Biol 24(9):3623–3632PubMedCrossRefGoogle Scholar
- Vertegaal AC, Ogg SC, Jaffray E, Rodriguez MS, Hay RT, Andersen JS, Mann M, Lamond AI (2004) A proteomic study of SUMO-2 target proteins. J Biol Chem 279(32):33791–33798. doi: 10.1074/jbc.M404201200 PubMedCrossRefGoogle Scholar
- Vertegaal AC, 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(12):2298–2310PubMedCrossRefGoogle Scholar
- Vethantham V, Manley JL (2009) Emerging roles for SUMO in mRNA processing and metabolism. In: Wilson, VG (ed) SUMO Regulation of Cellular Processes. Springer, pp 41–57Google Scholar
- Vethantham V, Rao N, Manley JL (2007) Sumoylation modulates the assembly and activity of the pre-mRNA 3' processing complex. Mol Cell Biol 27(24):8848–8858PubMedCrossRefGoogle Scholar
- Vethantham V, Rao N, Manley JL (2008) Sumoylation regulates multiple aspects of mammalian poly(A) polymerase function. Genes Dev 22(4):499–511PubMedCrossRefGoogle Scholar
- Vinciguerra P, Iglesias N, Camblong J, Zenklusen D, Stutz F (2005) Perinuclear Mlp proteins downregulate gene expression in response to a defect in mRNA export. EMBO J 24(4):813–823PubMedCrossRefGoogle Scholar
- Wang Z, Prelich G (2009) Quality control of a transcriptional regulator by SUMO-targeted degradation. Mol Cell Biol 29(7):1694–1706PubMedCrossRefGoogle Scholar
- Wei F, Scholer HR, Atchison ML (2007) Sumoylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem 282(29):21551–21560PubMedCrossRefGoogle Scholar
- Westman BJ, Verheggen C, Hutten S, Lam YW, Bertrand E, Lamond AI (2010) A proteomic screen for nucleolar SUMO targets shows SUMOylation modulates the function of Nop5/Nop58. Mol Cell 39(4):618–631PubMedCrossRefGoogle Scholar
- Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428(2):133–145PubMedCrossRefGoogle Scholar
- Wohlschlegel JA, Johnson ES, Reed SI, Yates JR 3rd (2004) Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279(44):45662–45668PubMedCrossRefGoogle Scholar
- Wotton D, Merrill JC (2007) Pc2 and SUMOylation. Biochem Soc Trans 35(Pt 6):1401–1404PubMedCrossRefGoogle Scholar
- Wykoff DD, O'Shea EK (2005) Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome. Mol Cell Proteomics 4(1):73–83PubMedGoogle Scholar
- Xie Y, Rubenstein EM, Matt T, Hochstrasser M (2010) SUMO-independent in vivo activity of a SUMO-targeted ubiquitin ligase toward a short-lived transcription factor. Genes Dev 24(9):893–903. doi: 10.1101/gad.1906510 PubMedCrossRefGoogle Scholar
- Zhao Y, Kwon SW, Anselmo A, Kaur K, White MA (2004) Broad spectrum identification of cellular small ubiquitin-related modifier (SUMO) substrate proteins. J Biol Chem 279(20):20999–21002. doi: 10.1074/jbc.M401541200 PubMedCrossRefGoogle Scholar
- 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(31):32262–32268. doi: 10.1074/jbc.M404173200 PubMedCrossRefGoogle Scholar