Screen for multi-SUMO-binding proteins reveals a multi-SIM-binding mechanism for recruitment of the transcriptional regulator ZMYM2 to chromatin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 35, 2015, Pages E4854-E4863

  Aguilar Martinez, Elisa ^a   Chen, Xi ^a   Webber, Aaron ^a   Mould, A Paul ^a   Seifert, Anne ^b   Hay, Ronald T ^b   Sharrocks, Andrew D ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Chromatin; SIM; SUMO; ZMYM2; ZNF198

Indexed keywords

BINDING PROTEIN; COREPRESSOR PROTEIN; PROTEIN ZMYM2; SUMO PROTEIN; UNCLASSIFIED DRUG; CHROMATIN; DNA BINDING PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR; ZMYM2 PROTEIN, HUMAN;

ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CHROMATIN; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SUMOYLATION; U2OS CELL LINE; HEK293 CELL LINE; METABOLISM;

CHROMATIN; DNA-BINDING PROTEINS; HEK293 CELLS; HUMANS; PROTEIN BINDING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION FACTORS;

EID: 84940972913     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509716112     Document Type: Article

References (55)

1. Heun P (2007) SUMOrganization of the nucleus. Curr Opin Cell Biol 19(3):350-355.
2. Finkbeiner E, Haindl M, Raman N, Muller S (2011) SUMO routes ribosome maturation. Nucleus 2(6):527-532.
3. Barry J, Lock RB (2011) Small ubiquitin-related modifier-1: Wrestling with protein regulation. Int J Biochem Cell Biol 43(1):37-40.
4. Cubeñas-Potts C, Matunis MJ (2013) SUMO: A multifaceted modifier of chromatin structure and function. Dev Cell 24(1):1-12.
5. Garcia-Dominguez M, Reyes JC (2009) SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 1789(6-8):451-459.
6. Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci USA 101(40):14373-14378.
7. Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I (2006) Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281(23):16117-16127.
8. Ulrich HD (2008) The fast-growing business of SUMO chains. Mol Cell 32(3):301-305.
9. Tatham MH, et al. (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10(5):538-546.
10. Lallemand-Breitenbach V, et al. (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10(5):547-555.
11. Bruderer R, et al. (2011) Purification and identification of endogenous polySUMO conjugates. EMBO Rep 12(2):142-148.
12. Srikumar T, et al. (2013) Global analysis of SUMO chain function reveals multiple roles in chromatin regulation. J Cell Biol 201(1):145-163.
13. Yang SH, Galanis A, Witty J, Sharrocks AD (2006) An extended consensus motif enhances the specificity of substrate modification by SUMO. EMBO J 25(21):5083-5093.
14. Nakagawa K, Kuzumaki N (2005) Transcriptional activity of megakaryoblastic leukemia 1 (MKL1) is repressed by SUMO modification. Genes Cells 10(8):835-850.
15. Kuo HY, et al. (2005) SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci USA 102(47):16973-16978.
16. Guo B, Sharrocks AD (2009) Extracellular signal-regulated kinase mitogen-activated protein kinase signaling initiates a dynamic interplay between sumoylation and ubiquitination to regulate the activity of the transcriptional activator PEA3. Mol Cell Biol 29(11):3204-3218.
17. Tammsalu T, et al. (2014) Proteome-wide identification of SUMO2 modification sites. Sci Signal 7(323):rs2.
18. Hendriks IA, et al. (2014) Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol 21(10):927-936.
19. Psakhye I, Jentsch S (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151(4):807-820.
20. Chen X, et al. (2013) The forkhead transcription factor FOXM1 controls cell cycle-dependent gene expression through an atypical chromatin binding mechanism. Mol Cell Biol 33(2):227-236.
21. Zhao Q, et al. (2014) GPS-SUMO: A tool for the prediction of sumoylation sites and SUMO-interaction motifs. Nucleic Acids Res 42(Web Server issue):W325-W330.
22. 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.
23. Malashkevich VN, Kammerer RA, Efimov VP, Schulthess T, Engel J (1996) The crystal structure of a five-stranded coiled coil in COMP: A prototype ion channel? Science 274(5288):761-765.
24. Zhu J, et al. (2008) Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J Biol Chem 283(43):29405-29415.
25. Ouyang J, Gill G (2009) SUMO engages multiple corepressors to regulate chromatin structure and transcription. Epigenetics 4(7):440-444.
26. Bastiani M, et al. (2009) MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 185(7):1259-1273.
27. Sekiyama N, et al. (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(51):35966-35975.
28. Shen LN, Dong C, Liu H, Naismith JH, Hay RT (2006) The structure of SENP1-SUMO-2 complex suggests a structural basis for discrimination between SUMO paralogues during processing. Biochem J 397(2):279-288.
29. Reverter D, Lima CD (2006) Structural basis for SENP2 protease interactions with SUMO precursors and conjugated substrates. Nat Struct Mol Biol 13(12):1060-1068.
30. Guzzo CM, et al. (2014) Characterization of the SUMO-binding activity of the myeloproliferative and mental retardation (MYM)-type zinc fingers in ZNF261 and ZNF198. PLoS One 9(8):e105271.
31. Malakhov MP, et al. (2004) SUMO fusions and SUMO-specific protease for efficient expression and purification of proteins. J Struct Funct Genomics 5(1-2):75-86.
32. 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(2):517-520.
33. Hakimi MA, Dong Y, Lane WS, Speicher DW, Shiekhattar R (2003) A candidate X-linked mental retardation gene is a component of a new family of histone deacetylase-containing complexes. J Biol Chem 278(9):7234-7239.
34. Shi YJ, et al. (2005) Regulation of LSD1 histone demethylase activity by its associated factors. Mol Cell 19(6):857-864.
35. Gocke CB, Yu H (2008) ZNF198 stabilizes the LSD1-CoREST-HDAC1 complex on chromatin through its MYM-type zinc fingers. PLoS One 3(9):e3255.
36. Seifert A, Schoefield P, Barton GJ, Hay RT (2015) Changes in the chromatin landscape of SUMO modification in response to proteotoxic stress. Sci Signal 8(384):rs7.
37. Kõivomägi M, et al. (2011) Cascades of multisite phosphorylation control Sic1 destruction at the onset of S phase. Nature 480(7375):128-131.
38. 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(5):610-619.
39. Rosendorff A, et al. (2006) NXP-2 association with SUMO-2 depends on lysines required for transcriptional repression. Proc Natl Acad Sci USA 103(14):5308-5313.
40. Xiao S, McCarthy JG, Aster JC, Fletcher JA (2000) ZNF198-FGFR1 transforming activity depends on a novel proline-rich ZNF198 oligomerization domain. Blood 96(2):699-704.
41. Ding H, et al. (2005) Solution structure of human SUMO-3 C47S and its binding surface for Ubc9. Biochemistry 44(8):2790-2799.
42. Witty J, Aguilar-Martinez E, Sharrocks AD (2010) SENP1 participates in the dynamic regulation of Elk-1 SUMOylation. Biochem J 428(2):247-254.
43. McMahon KA, et al. (2009) SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J 28(8):1001-1015.
44. Lemercier C, et al. (2000) mHDA1/HDAC5 histone deacetylase interacts with and represses MEF2A transcriptional activity. J Biol Chem 275(20):15594-15599.
45. Yang SH, Sharrocks AD (2010) The SUMO E3 ligase activity of Pc2 is coordinated through a SUMO interaction motif. Mol Cell Biol 30(9):2193-2205.
46. Lee TI, Johnstone SE, Young RA (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1(2):729-748.
47. Schmidt D, et al. (2009) ChIP-seq: Using high-throughput sequencing to discover protein-DNA interactions. Methods 48(3):240-248.
48. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25.
49. Heinz S, et al. (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38(4):576-589.
50. Kinsella RJ, et al. (2011) Ensembl BioMarts: A hub for data retrieval across taxonomic space. Database (Oxford) 2011:bar030.
51. Saldanha AJ (2004) Java Treeview - extensible visualization of microarray data. Bioinformatics 20(17):3246-3248.
52. Pearson RD, et al. (2009) puma: A Bioconductor package for propagating uncertainty in microarray analysis. BMC Bioinformatics 10:211.
53. Higgins SJ, Hames BD (1994) RNA Processing: A Practical Approach (IRL, Oxford), Vol I.
54. Tselepis VH, Green LJ, Humphries MJ (1997) An RGD to LDV motif conversion within the disintegrin kistrin generates an integrin antagonist that retains potency but exhibits altered receptor specificity. Evidence for a functional equivalence of acidic integrin-binding motifs. J Biol Chem 272(34):21341-21348.
55. Mellacheruvu D, et al. (2013) The CRAPome: A contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10(8):730-736.