An Acetylation Switch Regulates SUMO-Dependent Protein Interaction Networks

Molecular Cell

Volumn 46, Issue 6, 2012, Pages 759-770

  Ullmann, Rebecca ^a   Chien, Christopher D ^c   Avantaggiati, Maria Laura ^c   Muller, Stefan ^a,b  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAXX PROTEIN; GLUTAMINE; LYSINE; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO PROTEIN;

ACETYLATION; AMINO ACID SUBSTITUTION; ARTICLE; BINDING KINETICS; CELL NUCLEUS INCLUSION BODY; CONTROLLED STUDY; FEMALE; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; WILD TYPE;

ACETYLATION; BINDING SITES; GENE SILENCING; HEK293 CELLS; HELA CELLS; HISTONE DEACETYLASES; HUMANS; PROTEIN INTERACTION MAPS; SUMO-1 PROTEIN;

EID: 84863003858     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.04.006     Document Type: Article

References (66)

1. Baba D., Maita N., Jee J.G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 2005, 435:979-982.
2. Baba D., Maita N., Jee J.G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., Shirakawa M. Crystal structure of SUMO-3-modified thymine-DNA glycosylase. J. Mol. Biol. 2006, 359:137-147.
3. Bernardi R., Pandolfi P.P. Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat. Rev. Mol. Cell Biol. 2007, 8:1006-1016.
4. Chang C.C., Naik M.T., Huang Y.S., Jeng J.C., Liao P.H., Kuo H.Y., Ho C.C., Hsieh Y.L., Lin C.H., Huang N.J., et al. Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol. Cell 2011, 42:62-74.
5. Cheema A., Knights C.D., Rao M., Catania J., Perez R., Simons B., Dakshanamurthy S., Kolukula V.K., Tilli M., Furth P.A., et al. Functional mimicry of the acetylated C-terminal tail of p53 by a SUMO-1 acetylated domain, SAD. J. Cell. Physiol. 2010, 225:371-384.
6. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
7. Chupreta S., Holmstrom S., Subramanian L., Iniguez-Lluhi J.A. A small conserved surface in SUMO is the critical structural determinant of its transcriptional inhibitory properties. Mol. Cell. Biol. 2005, 25:4272-4282.
8. Deribe Y.L., Pawson T., Dikic I. Post-translational modifications in signal integration. Nat. Struct. Mol. Biol. 2010, 17:666-672.
9. Finkbeiner E., Haindl M., Muller S. The SUMO system controls nucleolar partitioning of a novel mammalian ribosome biogenesis complex. EMBO J. 2011, 30:1067-1078.
10. Gareau J.R., Lima C.D. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol. 2010, 11:861-871.
11. Geoffroy M.C., Hay R.T. An additional role for SUMO in ubiquitin-mediated proteolysis. Nat. Rev. Mol. Cell Biol. 2009, 10:564-568.
12. Gong L., Yeh E.T. Characterization of a family of nucleolar SUMO-specific proteases with preference for SUMO-2 or SUMO-3. J. Biol. Chem. 2006, 281:15869-15877.
13. Haindl M., Harasim T., Eick D., Muller S. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep. 2008, 9:273-279.
14. Hay R.T. SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 2007, 17:370-376.
15. Hecker C.M., Rabiller M., Haglund K., Bayer P., Dikic I. Specification of SUMO1- and SUMO2-interacting motifs. J. Biol. Chem. 2006, 281:16117-16127.
16. Huang W., Ghisletti S., Saijo K., Gandhi M., Aouadi M., Tesz G.J., Zhang D.X., Yao J., Czech M.P., Goode B.L., et al. Coronin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature 2011, 470:414-418.
17. Hunter T. The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol. Cell 2007, 28:730-738.
18. Ishov A.M., Sotnikov A.G., Negorev D., Vladimirova O.V., Neff N., Kamitani T., Yeh E.T., Strauss J.F., Maul G.G. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Biol. 1999, 147:221-234.
19. Jentsch S., Muller S. Regulatory functions of ubiquitin and SUMO in DNA repair pathways. Subcell. Biochem. 2011, 54:184-194.
20. Kamieniarz K., Schneider R. Tools to tackle protein acetylation. Chem. Biol. 2009, 16:1027-1029.
21. Kerscher O. SUMO junction-what's your function? New insights through SUMO-interacting motifs. EMBO Rep. 2007, 8:550-555.
22. Klein U.R., Haindl M., Nigg E.A., Muller S. RanBP2 and SENP3 function in a mitotic SUMO2/3 conjugation-deconjugation cycle on Borealin. Mol. Biol. Cell 2009, 20:410-418.
23. Kotaja N., Aittomaki S., Silvennoinen O., Palvimo J.J., Janne O.A. ARIP3 (androgen receptor-interacting protein 3) and other PIAS (protein inhibitor of activated STAT) proteins differ in their ability to modulate steroid receptor-dependent transcriptional activation. Mol. Endocrinol. 2000, 14:1986-2000.
24. Kotaja N., Karvonen U., Janne O.A., Palvimo J.J. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol. Cell. Biol. 2002, 22:5222-5234.
25. Ledl A., Schmidt D., Muller S. Viral oncoproteins E1A and E7 and cellular LxCxE proteins repress SUMO modification of the retinoblastoma tumor suppressor. Oncogene 2005, 24:3810-3818.
26. Lehembre F., Muller S., Pandolfi P.P., Dejean A. Regulation of Pax3 transcriptional activity by SUMO-1-modified PML. Oncogene 2001, 20:1-9.
27. 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., et al. Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol. Cell 2006, 24:341-354.
28. Mahajan R., Delphin C., Guan T., Gerace L., Melchior F. A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2. Cell 1997, 88:97-107.
29. Mahajan R., Gerace L., Melchior F. Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association. J. Cell Biol. 1998, 140:259-270.
30. Matunis M.J., Coutavas E., Blobel G. 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. 1996, 135:1457-1470.
31. Matunis M.J., Wu J., Blobel G. SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex. J. Cell Biol. 1998, 140:499-509.
32. Matunis M.J., Zhang X.D., Ellis N.A. SUMO: the glue that binds. Dev. Cell 2006, 11:596-597.
33. Mukhopadhyay D., Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem. Sci. 2007, 32:286-295.
34. Mukhopadhyay D., Matunis M.J. SUMmOning Daxx-mediated repression. Mol. Cell 2011, 42:4-5.
35. Muller S., Berger M., Lehembre F., Seeler J.S., Haupt Y., Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J. Biol. Chem. 2000, 275:13321-13329.
36. Namanja A.T., Li Y.J., Su Y., Wong S., Lu J., Colson L.T., Wu C., Li S.S., Chen Y. Insights into high affinity small ubiquitin-like modifier (SUMO) recognition by SUMO-interacting motifs (SIM) revealed by a combination of NMR and peptide array analysis. J. Biol. Chem. 2011, 287:3231-3240.
37. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
38. Neumann H., Hancock S.M., Buning R., Routh A., Chapman L., Somers J., Owen-Hughes T., van Noort J., Rhodes D., Chin J.W. A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol. Cell 2009, 36:153-163.
39. Ouyang J., Shi Y., Valin A., Xuan Y., Gill G. Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. Mol. Cell 2009, 34:145-154.
40. Palvimo J.J. PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans. 2007, 35:1405-1408.
41. Pascual G., Fong A.L., Ogawa S., Gamliel A., Li A.C., Perissi V., Rose D.W., Willson T.M., Rosenfeld M.G., Glass C.K. A SUMOylation-dependent pathway mediates transrepression of inflammatory response genes by PPAR-gamma. Nature 2005, 437:759-763.
42. Praefcke G.J., Hofmann K., Dohmen R.J. SUMO playing tag with ubiquitin. Trends Biochem. Sci. 2012, 37:23-31.
43. Reverter D., Lima C.D. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 2005, 435:687-692.
44. Rosendorff A., Sakakibara S., Lu S., Kieff E., Xuan Y., DiBacco A., Shi Y., Gill G. NXP-2 association with SUMO-2 depends on lysines required for transcriptional repression. Proc. Natl. Acad. Sci. USA 2006, 103:5308-5313.
45. Ruthenburg A.J., Li H., Patel D.J., Allis C.D. Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cell Biol. 2007, 8:983-994.
46. Rytinki M.M., Kaikkonen S., Pehkonen P., Jaaskelainen T., Palvimo J.J. PIAS proteins: pleiotropic interactors associated with SUMO. Cell. Mol. Life Sci. 2009, 66:3029-3041.
47. Schiller H.B., Friedel C.C., Boulegue C., Fassler R. Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 2011, 12:259-266.
48. Schmidt D., Muller S. Members of the PIAS family act as SUMO ligases for c-Jun and p53 and repress p53 activity. Proc. Natl. Acad. Sci. USA 2002, 99:2872-2877.
49. Schmidt D., Muller S. PIAS/SUMO: new partners in transcriptional regulation. Cell. Mol. Life Sci. 2003, 60:2561-2574.
50. Seet B.T., Dikic I., Zhou M.M., Pawson T. Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 2006, 7:473-483.
51. Sekiyama N., Ikegami T., Yamane T., Ikeguchi M., Uchimura Y., Baba D., Ariyoshi M., Tochio H., Saitoh H., Shirakawa M. Structure of the small ubiquitin-like modifier (SUMO)-interacting motif of MBD1-containing chromatin-associated factor 1 bound to SUMO-3. J. Biol. Chem. 2008, 283:35966-35975.
52. Shalizi A., Gaudilliere B., Yuan Z., Stegmuller J., Shirogane T., Ge Q., Tan Y., Schulman B., Harper J.W., Bonni A. A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science 2006, 311:1012-1017.
53. Shen T.H., Lin H.K., Scaglioni P.P., Yung T.M., Pandolfi P.P. The mechanisms of PML-nuclear body formation. Mol. Cell 2006, 24:331-339.
54. Song J., Durrin L.K., Wilkinson T.A., Krontiris T.G., Chen Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. USA 2004, 101:14373-14378.
55. Song J., Zhang Z., Hu W., Chen Y. Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J. Biol. Chem. 2005, 280:40122-40129.
56. Stehmeier P., Muller S. Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol. Cell 2009, 33:400-409.
57. Stielow B., Sapetschnig A., Kruger I., Kunert N., Brehm A., Boutros M., Suske G. Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. Mol. Cell 2008, 29:742-754.
58. Tatham M.H., Kim S., Jaffray E., Song J., Chen Y., Hay R.T. Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat. Struct. Mol. Biol. 2005, 12:67-74.
59. Taverna S.D., Li H., Ruthenburg A.J., Allis C.D., Patel D.J. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat. Struct. Mol. Biol. 2007, 14:1025-1040.
60. Van Nguyen T., Angkasekwinai P., Dou H., Lin F.M., Lu L.S., Cheng J., Chin Y.E., Dong C., Yeh E.T. SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Mol. Cell 2012, 45:210-221.
61. van Wijk S.J., Muller S., Dikic I. Shared and unique properties of ubiquitin and SUMO interaction networks in DNA repair. Genes Dev. 2011, 25:1763-1769.
62. Venteclef N., Jakobsson T., Ehrlund A., Damdimopoulos A., Mikkonen L., Ellis E., Nilsson L.M., Parini P., Janne O.A., Gustafsson J.A., et al. GPS2-dependent corepressor/SUMO pathways govern anti-inflammatory actions of LRH-1 and LXRbeta in the hepatic acute phase response. Genes Dev. 2010, 24:381-395.
63. Wilkinson K.A., Henley J.M. Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J. 2010, 428:133-145.
64. Zhong S., Muller S., Ronchetti S., Freemont P.S., Dejean A., Pandolfi P.P. Role of SUMO-1-modified PML in nuclear body formation. Blood 2000, 95:2748-2752.
65. Zhu J., Zhu S., Guzzo C.M., Ellis N.A., Sung K.S., Choi C.Y., Matunis M.J. Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 2008, 283:29405-29415.
66. Zhu S., Goeres J., Sixt K.M., Bekes M., Zhang X.D., Salvesen G.S., Matunis M.J. Protection from isopeptidase-mediated deconjugation regulates paralog-selective sumoylation of RanGAP1. Mol. Cell 2009, 33:570-580.