Structural and Functional Characterization of the Phosphorylation-Dependent Interaction between PML and SUMO1

Structure

Volumn 23, Issue 1, 2015, Pages 126-138

  Cappadocia, Laurent ^a,c   Mascle, Xavier H ^a,c   Bourdeau, Véronique ^a   Tremblay Belzile, Samuel ^a   Chaker Margot, Malik ^a   Lussier Price, Mathieu ^a   Wada, Junya ^b   Sakaguchi, Kazuyasu ^b   Aubry, Muriel ^a   Ferbeyre, Gerardo ^a   Omichinski, James G ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b HOKKAIDO UNIVERSITY   (Japan)

^c NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE TRIPHOSPHATE; FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; SARM1 PROTEIN; UNCLASSIFIED DRUG; DAXX PROTEIN, HUMAN; NUCLEAR PROTEIN; PML PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SUMO 1 PROTEIN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; CONTROLLED STUDY; ENERGY; ENZYME ACTIVATION; HOMEOSTASIS; MORPHOLOGY; MOUSE; NERVE FIBER; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SUMO-1 PROTEIN; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84920994917     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.10.015     Document Type: Article

References (45)

1. A.A. Armstrong, F. Mohideen, and C.D. Lima Recognition of SUMO-modified PCNA requires tandem receptor motifs in Srs2 Nature 483 2012 59 63
2. O. Bischof, O. Kirsh, M. Pearson, K. Itahana, P.G. Pelicci, and A. Dejean Deconstructing PML-induced premature senescence EMBO J. 21 2002 3358 3369
3. C.-C. Chang, M.T. Naik, Y.-S. Huang, J.-C. Jeng, P.-H. Liao, H.-Y. Kuo, C.-C. Ho, Y.-L. Hsieh, C.-H. Lin, and N.-J. Huang Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation Mol. Cell 42 2011 62 74
4. A. Cheema, C.D. Knights, M. Rao, J. Catania, R. Perez, B. Simons, S. Dakshanamurthy, V.K. Kolukula, M. Tilli, and P.A. Furth Functional mimicry of the acetylated C-terminal tail of p53 by a SUMO-1 acetylated domain, SAD J. Cell. Physiol. 225 2010 371 384
5. Y.-C.M. Chen, C. Kappel, J. Beaudouin, R. Eils, and D.L. Spector Live cell dynamics of promyelocytic leukemia nuclear bodies upon entry into and exit from mitosis Mol. Biol. Cell 19 2008 3147 3162
6. G. Cho, Y. Lim, and J.A. Golden SUMO interaction motifs in Sizn1 are required for promyelocytic leukemia protein nuclear body localization and for transcriptional activation J. Biol. Chem. 284 2009 19592 19600
7. C. Choudhary, C. Kumar, F. Gnad, M.L. Nielsen, M. Rehman, T.C. Walther, J.V. Olsen, and M. Mann Lysine acetylation targets protein complexes and co-regulates major cellular functions Science 325 2009 834 840
8. J.R. Danielsen, L.K. Povlsen, B.H. Villumsen, W. Streicher, J. Nilsson, M. Wikström, S. Bekker-Jensen, and N. Mailand DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger J. Cell Biol. 197 2012 179 187
9. G. Dellaire, and D.P. Bazett-Jones Beyond repair foci: subnuclear domains and the cellular response to DNA damage Cell Cycle 6 2007 1864 1872
10. G. Dellaire, R.W. Ching, K. Ahmed, F. Jalali, K.C.K. Tse, R.G. Bristow, and D.P. Bazett-Jones Promyelocytic leukemia nuclear bodies behave as DNA damage sensors whose response to DNA double-strand breaks is regulated by NBS1 and the kinases ATM, Chk2, and ATR J. Cell Biol. 175 2006 55 66
11. J.M.P. Desterro, M.S. Rodriguez, G.D. Kemp, and R.T. Hay Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1 J. Biol. Chem. 274 1999 10618 10624
12. R.D. Everett, P. Lomonte, T. Sternsdorf, R. van Driel, and A. Orr Cell cycle regulation of PML modification and ND10 composition J. Cell Sci. 112 1999 4581 4588
13. G. Ferbeyre, E. de Stanchina, E. Querido, N. Baptiste, C. Prives, and S.W. Lowe PML is induced by oncogenic ras and promotes premature senescence Genes Dev. 14 2000 2015 2027
14. J.R. Gareau, and C.D. Lima The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition Nat. Rev. Mol. Cell Biol. 11 2010 861 871
15. J.R. Gareau, D. Reverter, and C.D. Lima Determinants of small ubiquitin-like modifier 1 (SUMO1) protein specificity, E3 ligase, and SUMO-RanGAP1 binding activities of nucleoporin RanBP2 J. Biol. Chem. 287 2012 4740 4751
16. C.M. Hecker, M. Rabiller, K. Haglund, P. Bayer, and I. Dikic Specification of SUMO1- and SUMO2-interacting motifs J. Biol. Chem. 281 2006 16117 16127
17. K. Husnjak, and I. Dikic Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions Annu. Rev. Biochem. 81 2012 291 322
18. A.M. Ishov, A.G. Sotnikov, D. Negorev, O.V. Vladimirova, N. Neff, T. Kamitani, E.T.H. Yeh, J.F. Strauss 3rd, and G.G. Maul 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. 147 1999 221 234
19. K. Jensen, C. Shiels, and P.S. Freemont PML protein isoforms and the RBCC/TRIM motif Oncogene 20 2001 7223 7233
20. T. Kahyo, T. Nishida, and H. Yasuda Involvement of PIAS1 in the sumoylation of tumor suppressor p53 Mol. Cell 8 2001 713 718
21. V. Lallemand-Breitenbach, and H. de Thé PML nuclear bodies Cold Spring Harb. Perspect. Biol. 2 2010 a000661
22. D.-Y. Lin, Y.-S. Huang, J.-C. Jeng, H.-Y. Kuo, C.-C. Chang, T.-T. Chao, C.-C. Ho, Y.-C. Chen, T.-P. Lin, and H.-I. Fang Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors Mol. Cell 24 2006 341 354
23. M.A. Maroui, S. Kheddache-Atmane, F. El Asmi, L. Dianoux, M. Aubry, and M.K. Chelbi-Alix Requirement of PML SUMO interacting motif for RNF4- or arsenic trioxide-induced degradation of nuclear PML isoforms PLoS ONE 7 2012 e44949
24. X.H. Mascle, D. Germain-Desprez, P. Huynh, P. Estephan, and M. Aubry Sumoylation of the transcriptional intermediary factor 1beta (TIF1beta), the Co-repressor of the KRAB Multifinger proteins, is required for its transcriptional activity and is modulated by the KRAB domain J. Biol. Chem. 282 2007 10190 10202
25. D. Negorev, A.M. Ishov, and G.G. Maul Evidence for separate ND10-binding and homo-oligomerization domains of Sp100 J. Cell Sci. 114 2001 59 68
26. S.K. Olsen, A.D. Capili, X. Lu, D.S. Tan, and C.D. Lima Active site remodelling accompanies thioester bond formation in the SUMO E1 Nature 463 2010 906 912
27. Y. Percherancier, D. Germain-Desprez, F. Galisson, X.H. Mascle, L. Dianoux, P. Estephan, M.K. Chelbi-Alix, and M. Aubry Role of SUMO in RNF4-mediated promyelocytic leukemia protein (PML) degradation: sumoylation of PML and phospho-switch control of its SUMO binding domain dissected in living cells J. Biol. Chem. 284 2009 16595 16608
28. A. Pichler, A. Gast, J.S. Seeler, A. Dejean, and F. Melchior The nucleoporin RanBP2 has SUMO1 E3 ligase activity Cell 108 2002 109 120
29. A. Rabellino, B. Carter, G. Konstantinidou, S.-Y. Wu, A. Rimessi, L.A. Byers, J.V. Heymach, L. Girard, C.-M. Chiang, J. Teruya-Feldstein, and P.P. Scaglioni The SUMO E3-ligase PIAS1 regulates the tumor suppressor PML and its oncogenic counterpart PML-RARA Cancer Res. 72 2012 2275 2284
30. Z.A. Rasheed, A. Saleem, Y. Ravee, P.P. Pandolfi, and E.H. Rubin The topoisomerase I-binding RING protein, topors, is associated with promyelocytic leukemia nuclear bodies Exp. Cell Res. 277 2002 152 160
31. D. Reverter, and C.D. Lima Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex Nature 435 2005 687 692
32. P. Salomoni, R. Bernardi, S. Bergmann, A. Changou, S. Tuttle, and P.P. Pandolfi The promyelocytic leukemia protein PML regulates c-Jun function in response to DNA damage Blood 105 2005 3686 3690
33. P. Salomoni, M. Dvorkina, and D. Michod Role of the promyelocytic leukaemia protein in cell death regulation Cell Death Dis. 3 2012 e247
34. P.P. Scaglioni, T.M. Yung, L.F. Cai, H. Erdjument-Bromage, A.J. Kaufman, B. Singh, J. Teruya-Feldstein, P. Tempst, and P.P. Pandolfi A CK2-dependent mechanism for degradation of the PML tumor suppressor Cell 126 2006 269 283
35. P.P. Scaglioni, T.M. Yung, S. Choi, C. Baldini, G. Konstantinidou, and P.P. Pandolfi CK2 mediates phosphorylation and ubiquitin-mediated degradation of the PML tumor suppressor Mol. Cell. Biochem. 316 2008 149 154
36. N. Sekiyama, T. Ikegami, T. Yamane, M. Ikeguchi, Y. Uchimura, D. Baba, M. Ariyoshi, H. Tochio, H. Saitoh, and M. Shirakawa 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 2008 35966 35975
37. L.N. Shen, C. Dong, H. Liu, J.H. Naismith, and R.T. Hay The structure of SENP1-SUMO-2 complex suggests a structural basis for discrimination between SUMO paralogues during processing Biochem. J. 397 2006 279 288
38. J. Song, L.K. Durrin, T.A. Wilkinson, T.G. Krontiris, and Y. Chen Identification of a SUMO-binding motif that recognizes SUMO-modified proteins Proc. Natl. Acad. Sci. USA 101 2004 14373 14378
39. J. Song, Z. Zhang, W. Hu, and Y. Chen Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation J. Biol. Chem. 280 2005 40122 40129
40. P. Stehmeier, and S. Muller Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling Mol. Cell 33 2009 400 409
41. K.S. Sung, Y.-A. Lee, E.T. Kim, S.-R. Lee, J.-H. Ahn, and C.Y. Choi Role of the SUMO-interacting motif in HIPK2 targeting to the PML nuclear bodies and regulation of p53 Exp. Cell Res. 317 2011 1060 1070
42. R. Ullmann, C.D. Chien, M.L. Avantaggiati, and S. Muller An acetylation switch regulates SUMO-dependent protein interaction networks Mol. Cell 46 2012 759 770
43. M. Vernier, V. Bourdeau, M.-F. Gaumont-Leclerc, O. Moiseeva, V. Bégin, F. Saad, A.-M. Mes-Masson, and G. Ferbeyre Regulation of E2Fs and senescence by PML nuclear bodies Genes Dev. 25 2011 41 50
44. S. Weidtkamp-Peters, T. Lenser, D. Negorev, N. Gerstner, T.G. Hofmann, G. Schwanitz, C. Hoischen, G. Maul, P. Dittrich, and P. Hemmerich Dynamics of component exchange at PML nuclear bodies J. Cell Sci. 121 2008 2731 2743
45. S. Zhong, P. Salomoni, and P.P. Pandolfi The transcriptional role of PML and the nuclear body Nat. Cell Biol. 2 2000 E85 E90