Requirement of PML SUMO Interacting Motif for RNF4- or Arsenic Trioxide-Induced Degradation of Nuclear PML Isoforms

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Maroui, Mohamed Ali ^a   Kheddache Atmane, Sabrina ^a   El Asmi, Faten ^a   Dianoux, Laurent ^a   Aubry, Muriel ^b   Chelbi Alix, Mounira K ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC TRIOXIDE; ISOPROTEIN; PROMYELOCYTIC LEUKEMIA PROTEIN; PROTEASOME; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CARBOXY TERMINAL SEQUENCE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SENSITIVITY ANALYSIS; SUMOYLATION; UBIQUITINATION;

AMINO ACID MOTIFS; ANIMALS; ARSENICALS; CELL LINE, TUMOR; CELL NUCLEUS; CYTOPLASM; HUMANS; MICE; MUTATION; NUCLEAR PROTEINS; OXIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEOLYSIS; SUMO-1 PROTEIN; SUMOYLATION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84866510150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044949     Document Type: Article

References (59)

1. Ishov AM, Sotnikov AG, Negorev D, Vladimirova OV, Neff N, et al. (1999) 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: 221-234.
2. Geoffroy MC, Chelbi-Alix MK, (2011) Role of promyelocytic leukemia protein in host antiviral defense. J Interferon Cytokine Res 31: 145-158.
3. Bernardi R, Papa A, Pandolfi PP, (2008) Regulation of apoptosis by PML and the PML-NBs. Oncogene 27: 6299-6312.
4. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, et al. (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10: 538-546.
5. Lallemand-Breitenbach V, Zhu J, Puvion F, Koken M, Honore N, et al. (2001) Role of promyelocytic leukemia (PML) sumolation in nuclear body formation, 11S proteasome recruitment, and As2O3-induced PML or PML/retinoic acid receptor alpha degradation. J Exp Med 193: 1361-1371.
6. Pampin M, Simonin Y, Blondel B, Percherancier Y, Chelbi-Alix MK, (2006) Cross talk between PML and p53 during poliovirus infection: implications for antiviral defense. J Virol 80: 8582-8592.
7. El McHichi B, Regad T, Maroui MA, Rodriguez MS, Aminev A, et al. (2010) SUMOylation promotes PML degradation during encephalomyocarditis virus infection. J Virol 84: 11634-11645.
8. Everett RD, Chelbi-Alix MK, (2007) PML and PML nuclear bodies: implications in antiviral defence. Biochimie 89: 819-830.
9. Krieghoff-Henning E, Hofmann TG, (2008) Role of nuclear bodies in apoptosis signalling. Biochim Biophys Acta 1783: 2185-2194.
10. Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, et al. (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10: 547-555.
11. Van Damme E, Laukens K, Dang TH, Van Ostade X, (2010) A manually curated network of the PML nuclear body interactome reveals an important role for PML-NBs in SUMOylation dynamics. Int J Biol Sci 6: 51-67.
12. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, et al. (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15: 3088-3103.
13. Best JL, Ganiatsas S, Agarwal S, Changou A, Salomoni P, et al. (2002) SUMO-1 protease-1 regulates gene transcription through PML. Mol Cell 10: 843-855.
14. Kamitani T, Kito K, Nguyen HP, Wada H, Fukuda-Kamitani T, et al. (1998) Identification of three major sentrinization sites in PML. J Biol Chem 273: 26675-26682.
15. Muller S, Matunis MJ, Dejean A, (1998) Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J 17: 61-70.
16. Percherancier Y, Germain-Desprez D, Galisson F, Mascle XH, Dianoux L, et al. (2009) 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: 16595-16608.
17. Zhu J, Koken MH, Quignon F, Chelbi-Alix MK, Degos L, et al. (1997) Arsenic-induced PML targeting onto nuclear bodies: implications for the treatment of acute promyelocytic leukemia. Proc Natl Acad Sci U S A 94: 3978-3983.
18. Hayakawa F, Privalsky ML, (2004) Phosphorylation of PML by mitogen-activated protein kinases plays a key role in arsenic trioxide-mediated apoptosis. Cancer Cell 5: 389-401.
19. Zhang XW, Yan XJ, Zhou ZR, Yang FF, Wu ZY, et al. (2010) Arsenic trioxide controls the fate of the PML-RARalpha oncoprotein by directly binding PML. Science 328: 240-243.
20. Weisshaar SR, Keusekotten K, Krause A, Horst C, Springer HM, et al. (2008) Arsenic trioxide stimulates SUMO-2/3 modification leading to RNF4-dependent proteolytic targeting of PML. FEBS Lett 582: 3174-3178.
21. Perry JJ, Tainer JA, Boddy MN, (2008) A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 33: 201-208.
22. Chiariotti L, Benvenuto G, Fedele M, Santoro M, Simeone A, et al. (1998) Identification and characterization of a novel RING-finger gene (RNF4) mapping at 4p16.3. Genomics 47: 258-265.
23. Hakli M, Karvonen U, Janne OA, Palvimo JJ, (2005) SUMO-1 promotes association of SNURF (RNF4) with PML nuclear bodies. Exp Cell Res 304: 224-233.
24. Moilanen AM, Poukka H, Karvonen U, Hakli M, Janne OA, et al. (1998) Identification of a novel RING finger protein as a coregulator in steroid receptor-mediated gene transcription. Mol Cell Biol 18: 5128-5139.
25. Rabellino A, Carter BJ, Konstantinidou G, Shwu-Yuan W, Rimessi A, et al. (2012) The SUMO E3-ligase PIAS1 regulates the tumor suppressor PML and its oncogenic counterpart PML-RARA. Cancer Res [Epub ahead of print].
26. Jensen K, Shiels C, Freemont PS, (2001) PML protein isoforms and the RBCC/TRIM motif. Oncogene 20: 7223-7233.
27. Bernardi R, Pandolfi PP, (2007) Structure, dynamics and functions of promyelocytic leukaemia nuclear bodies. Nat Rev Mol Cell Biol 8: 1006-1016.
28. Wei X, Yu ZK, Ramalingam A, Grossman SR, Yu JH, et al. (2003) Physical and functional interactions between PML and MDM2. J Biol Chem 278: 29288-29297.
29. Fogal V, Gostissa M, Sandy P, Zacchi P, Sternsdorf T, et al. (2000) Regulation of p53 activity in nuclear bodies by a specific PML isoform. EMBO J 19: 6185-6195.
30. Henderson BR, Eleftheriou A, (2000) A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Exp Cell Res 256: 213-224.
31. Condemine W, Takahashi Y, Le Bras M, de The H, (2007) A nucleolar targeting signal in PML-I addresses PML to nucleolar caps in stressed or senescent cells. J Cell Sci 120: 3219-3227.
32. Shen TH, Lin HK, Scaglioni PP, Yung TM, Pandolfi PP, (2006) The mechanisms of PML-nuclear body formation. Mol Cell 24: 331-339.
33. Stehmeier P, Muller S, (2009) Phospho-regulated SUMO interaction modules connect the SUMO system to CK2 signaling. Mol Cell 33: 400-409.
34. Condemine W, Takahashi Y, Zhu J, Puvion-Dutilleul F, Guegan S, et al. (2006) Characterization of endogenous human promyelocytic leukemia isoforms. Cancer Res 66: 6192-6198.
35. Brand P, Lenser T, Hemmerich P, (2010) Assembly dynamics of PML nuclear bodies in living cells. PMC Biophys 3: 3.
36. Germain-Desprez D, Bazinet M, Bouvier M, Aubry M, (2003) Oligomerization of transcriptional intermediary factor 1 regulators and interaction with ZNF74 nuclear matrix protein revealed by bioluminescence resonance energy transfer in living cells. J Biol Chem 278: 22367-22373.
37. Xu Y, Piston DW, Johnson CH, (1999) A bioluminescence resonance energy transfer (BRET) system: application to interacting circadian clock proteins. Proc Natl Acad Sci U S A 96: 151-156.
38. Angers S, Salahpour A, Joly E, Hilairet S, Chelsky D, et al. (2000) Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc Natl Acad Sci U S A 97: 3684-3689.
39. Blondel D, Kheddache S, Lahaye X, Dianoux L, Chelbi-Alix MK, (2010) Resistance to rabies virus infection conferred by the PMLIV isoform. J Virol 84: 10719-10726.
40. Perroy J, Pontier S, Charest PG, Aubry M, Bouvier M, (2004) Real-time monitoring of ubiquitination in living cells by BRET. Nat Methods 1: 203-208.
41. Nervi C, Ferrara FF, Fanelli M, Rippo MR, Tomassini B, et al. (1998) Caspases mediate retinoic acid-induced degradation of the acute promyelocytic leukemia PML/RARalpha fusion protein. Blood 92: 2244-2251.
42. Chelbi-Alix MK, Pelicano L, Quignon F, Koken MH, Venturini L, et al. (1995) Induction of the PML protein by interferons in normal and APL cells. Leukemia 9: 2027-2033.
43. de la Vega L, Frobius K, Moreno R, Calzado MA, Geng H, et al. (2011) Control of nuclear HIPK2 localization and function by a SUMO interaction motif. Biochim Biophys Acta 1813: 283-297.
44. Lin DY, Huang YS, Jeng JC, Kuo HY, Chang CC, et al. (2006) Role of SUMO-interacting motif in Daxx SUMO modification, subnuclear localization, and repression of sumoylated transcription factors. Mol Cell 24: 341-354.
45. Zhu J, Zhu S, Guzzo CM, Ellis NA, Sung KS, et al. (2008) Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J Biol Chem 283: 29405-29415.
46. Chang CC, Naik MT, Huang YS, Jeng JC, Liao PH, et al. (2011) Structural and Functional Roles of Daxx SIM Phosphorylation in SUMO Paralog-Selective Binding and Apoptosis Modulation. Mol Cell 42: 62-74.
47. Escobar-Cabrera E, Okon M, Lau DK, Dart CF, Bonvin AM, et al. (2011) Characterizing the N- and C-terminal Small ubiquitin-like modifier (SUMO)-interacting motifs of the scaffold protein DAXX. J Biol Chem 286: 19816-19829.
48. Geoffroy MC, Jaffray EG, Walker KJ, Hay RT, (2010) Arsenic-induced SUMO-dependent recruitment of RNF4 into PML nuclear bodies. Mol Biol Cell 21: 4227-4239.
49. Dacres H, Dumancic MM, Horne I, Trowell SC, (2009) Direct comparison of fluorescence- and bioluminescence-based resonance energy transfer methods for real-time monitoring of thrombin-catalysed proteolytic cleavage. Biosens Bioelectron 24: 1164-1170.
50. Dacres H, Dumancic MM, Horne I, Trowell SC, (2009) Direct comparison of bioluminescence-based resonance energy transfer methods for monitoring of proteolytic cleavage. Anal Biochem 385: 194-202.
51. Sung KS, Lee YA, Kim ET, Lee SR, Ahn JH, et al. (2011) Role of the SUMO-interacting motif in HIPK2 targeting to the PML nuclear bodies and regulation of p53. Exp Cell Res 317: 1060-1070.
52. Peche LY, Scolz M, Ladelfa MF, Monte M, Schneider C (2011) MageA2 restrains cellular senescence by targeting the function of PMLIV/p53 axis at the PML-NBs. Cell Death Differ.
53. Cuchet D, Sykes A, Nicolas A, Orr A, Murray J, et al. (2011) PML isoforms I and II participate in PML-dependent restriction of HSV-1 replication. J Cell Sci 124: 280-291.
54. Cuchet-Lourenco D, Boutell C, Lukashchuk V, Grant K, Sykes A, et al. (2011) SUMO pathway dependent recruitment of cellular repressors to herpes simplex virus type 1 genomes. PLoS Pathog 7: e1002123.
55. Boutell C, Cuchet-Lourenco D, Vanni E, Orr A, Glass M, et al. (2011) A viral ubiquitin ligase has substrate preferential SUMO targeted ubiquitin ligase activity that counteracts intrinsic antiviral defence. PLoS Pathog 7: e1002245.
56. Kaiser FJ, Moroy T, Chang GT, Horsthemke B, Ludecke HJ, (2003) The RING finger protein RNF4, a co-regulator of transcription, interacts with the TRPS1 transcription factor. J Biol Chem 278: 38780-38785.
57. Ayaydin F, Dasso M, (2004) Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 15: 5208-5218.
58. Wang ZG, Ruggero D, Ronchetti S, Zhong S, Gaboli M, et al. (1998) PML is essential for multiple apoptotic pathways. Nat Genet 20: 266-272.
59. Galisson F, Mahrouche L, Courcelles M, Bonneil E, Meloche S, et al. (2010) A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol Cell Proteomics.