The chromatin modification by SUMO-2/3 but not SUMO-1 prevents the epigenetic activation of key immune-related genes during Kaposi's sarcoma associated herpesvirus reactivation

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Chang, Pei Ching ^a   Cheng, Chia Yang ^b   Campbell, Mel ^c   Yang, Yi Cheng ^a   Hsu, Hung Wei ^a   Chang, Ting Yu ^a   Chu, Chia Han ^b   Lee, Yi Wei ^a   Hung, Chiu Lien ^d   Lai, Shi Mei ^b   Tepper, Clifford G ^c,e   Hsieh, Wen Ping ^b   Wang, Hsei Wei ^a   Tang, Chuan Yi ^b   Wang, Wen Ching ^b   Kung, Hsing Jien ^c,d,e,f  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CD40 LIGAND; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FOCAL ADHESION KINASE; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; INTERFERON REGULATORY FACTOR 7; MYC PROTEIN; MYOCYTE ENHANCER FACTOR 2; PROLACTIN; PROTEIN P53; STAT1 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; STAT6 PROTEIN; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR E2F4; TRANSCRIPTION FACTOR E2F5; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR PBX1; UBIQUITIN PROTEIN LIGASE E3; UPSTREAM STIMULATORY FACTOR 1; CHROMATIN; INTERFERON REGULATORY FACTOR; PROTEIN BINDING; SUMO PROTEIN; SUMO2 PROTEIN, HUMAN; SUMO3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; UBIQUITIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; EPIGENETICS; GENE ACTIVATION; HERPES VIRUS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; IMMUNOSURVEILLANCE; KAPOSI SARCOMA; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION REGULATION; UPREGULATION; VIRUS REACTIVATION; WESTERN BLOTTING; CHROMATIN; GENE; GENE ONTOLOGY; GENETIC EPIGENESIS; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY; VIRUS ACTIVATION;

EUKARYOTA; HERPESVIRIDAE; HUMAN HERPESVIRUS 8; MAMMALIA;

CELL LINE, TUMOR; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; EPIGENESIS, GENETIC; GENE ONTOLOGY; GENES, MHC CLASS II; HEK293 CELLS; HERPESVIRUS 8, HUMAN; HUMANS; INTERFERON REGULATORY FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TRANSCRIPTION FACTORS; TRANSCRIPTOME; UBIQUITINS; VIRUS ACTIVATION;

EID: 84887966627     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-824     Document Type: Article

References (55)

1. Lomeli H, Vazquez M. Emerging roles of the SUMO pathway in development. Cell Mol Life Sci 2011, 68:4045-4064. 10.1007/s00018-011-0792-5, 21892772.
2. Nacerddine K, Lehembre F, Bhaumik M, Artus J, Cohen-Tannoudji M, Babinet C, Pandolfi PP, Dejean A. The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev Cell 2005, 9:769-779. 10.1016/j.devcel.2005.10.007, 16326389.
3. Prudden J, Perry JJ, Nie M, Vashisht AA, Arvai AS, Hitomi C, Guenther G, Wohlschlegel JA, Tainer JA, Boddy MN. DNA repair and global sumoylation are regulated by distinct Ubc9 noncovalent complexes. Mol Cell Biol 2011, 31:2299-2310. 10.1128/MCB.05188-11, 3133251, 21444718.
4. Garcia-Dominguez M, Reyes JC. SUMO association with repressor complexes, emerging routes for transcriptional control. Biochim Biophys Acta 2009, 1789:451-459. 10.1016/j.bbagrm.2009.07.001, 19616654.
5. Wilkinson KA, Henley JM. Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 2010, 428:133-145. 10.1042/BJ20100158, 3310159, 20462400.
6. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G. SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 2011, 43:220-227. 10.1038/ng.765, 21317888.
7. Rosonina E, Duncan SM, Manley JL. SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev 2010, 24:1242-1252. 10.1101/gad.1917910, 2885660, 20504900.
8. Makhnevych T, Sydorskyy Y, Xin X, Srikumar T, Vizeacoumar FJ, Jeram SM, Li Z, Bahr S, Andrews BJ, Boone C, Raught B. Global map of SUMO function revealed by protein-protein interaction and genetic networks. Mol Cell 2009, 33:124-135. 10.1016/j.molcel.2008.12.025, 19150434.
9. Tatham MH, Jaffray E, Vaughan OA, Desterro JM, Botting CH, Naismith JH, Hay RT. Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J Biol Chem 2001, 276:35368-35374. 10.1074/jbc.M104214200, 11451954.
10. Matic I, van Hagen M, Schimmel J, Macek B, Ogg SC, Tatham MH, Hay RT, Lamond AI, Mann M, Vertegaal AC. In vivo identification of human small ubiquitin-like modifier polymerization sites by high accuracy mass spectrometry and an in vitro to in vivo strategy. Mol Cell Proteomics 2008, 7:132-144. 3840926, 17938407.
11. Saitoh H, Hinchey J. Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 2000, 275:6252-6258. 10.1074/jbc.275.9.6252, 10692421.
12. Ayaydin F, Dasso M. Distinct in vivo dynamics of vertebrate SUMO paralogues. Mol Biol Cell 2004, 15:5208-5218. 10.1091/mbc.E04-07-0589, 532004, 15456902.
13. Kolli N, Mikolajczyk J, Drag M, Mukhopadhyay D, Moffatt N, Dasso M, Salvesen G, Wilkinson KD. Distribution and paralogue specificity of mammalian deSUMOylating enzymes. Biochem J 2010, 430:335-344. 10.1042/BJ20100504, 3749516, 20590526.
14. Lin DY, Huang YS, Jeng JC, Kuo HY, Chang CC, Chao TT, Ho CC, Chen YC, Lin TP, Fang HI, 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. 10.1016/j.molcel.2006.10.019, 17081986.
15. Namanja AT, Li YJ, Su Y, Wong S, Lu J, Colson LT, Wu C, Li SS, Chen Y. Insights into high affinity small ubiquitin-like modifier (SUMO) recognition by SUMO-interacting motifs (SIMs) revealed by a combination of NMR and peptide array analysis. J Biol Chem 2012, 287:3231-3240. 10.1074/jbc.M111.293118, 3270977, 22147707.
16. Chang PC, Izumiya Y, Wu CY, Fitzgerald LD, Campbell M, Ellison TJ, Lam KS, Luciw PA, Kung HJ. Kaposi's sarcoma-associated herpesvirus (KSHV) encodes a SUMO E3 ligase that is SIM-dependent and SUMO-2/3-specific. J Biol Chem 2010, 285:5266-5273. 10.1074/jbc.M109.088088, 2820755, 20034935.
17. Gareau JR, Reverter D, Lima CD. Determinants of small ubiquitin-like modifier 1 (SUMO1) protein specificity, E3 ligase, and SUMO-RanGAP1 binding activities of nucleoporin RanBP2. J Biol Chem 2012, 287:4740-4751. 10.1074/jbc.M111.321141, 3281653, 22194619.
18. Tatham MH, Kim S, Jaffray E, Song J, Chen Y, Hay RT. Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat Struct Mol Biol 2005, 12:67-74. 10.1038/nsmb878, 15608651.
19. Meulmeester E, Kunze M, Hsiao HH, Urlaub H, Melchior F. Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol Cell 2008, 30:610-619. 10.1016/j.molcel.2008.03.021, 18538659.
20. Bailey D, O'Hare P. Herpes simplex virus 1 ICP0 co-localizes with a SUMO-specific protease. J Gen Virol 2002, 83:2951-2964.
21. Boggio R, Chiocca S. Viruses and sumoylation: recent highlights. Curr Opin Microbiol 2006, 9:430-436. 10.1016/j.mib.2006.06.008, 16815735.
22. Boggio R, Colombo R, Hay RT, Draetta GF, Chiocca S. A mechanism for inhibiting the SUMO pathway. Mol Cell 2004, 16:549-561. 10.1016/j.molcel.2004.11.007, 15546615.
23. Chang PC, Fitzgerald LD, Van Geelen A, Izumiya Y, Ellison TJ, Wang DH, Ann DK, Luciw PA, Kung HJ. Kruppel-associated box domain-associated protein-1 as a latency regulator for Kaposi's sarcoma-associated herpesvirus and its modulation by the viral protein kinase. Cancer Res 2009, 69:5681-5689. 10.1158/0008-5472.CAN-08-4570, 2731626, 19584288.
24. Chang TH, Kubota T, Matsuoka M, Jones S, Bradfute SB, Bray M, Ozato K. Ebola Zaire virus blocks type I interferon production by exploiting the host SUMO modification machinery. PLoS Pathog 2009, 5:e1000493. 10.1371/journal.ppat.1000493, 2696038, 19557165.
25. Izumiya Y, Ellison TJ, Yeh ET, Jung JU, Luciw PA, Kung HJ. Kaposi's sarcoma-associated herpesvirus K-bZIP represses gene transcription via SUMO modification. J Virol 2005, 79:9912-9925. 10.1128/JVI.79.15.9912-9925.2005, 1181544, 16014952.
26. Adamson AL, Kenney S. Epstein-barr virus immediate-early protein BZLF1 is SUMO-1 modified and disrupts promyelocytic leukemia bodies. J Virol 2001, 75:2388-2399. 10.1128/JVI.75.5.2388-2399.2001, 114822, 11160742.
27. Chang LK, Lee YH, Cheng TS, Hong YR, Lu PJ, Wang JJ, Wang WH, Kuo CW, Li SS, Liu ST. Post-translational modification of Rta of Epstein-Barr virus by SUMO-1. J Biol Chem 2004, 279:38803-38812. 10.1074/jbc.M405470200, 15229220.
28. Chang LK, Liu ST, Kuo CW, Wang WH, Chuang JY, Bianchi E, Hong YR. Enhancement of transactivation activity of Rta of Epstein-Barr virus by RanBPM. J Mol Biol 2008, 379:231-242. 10.1016/j.jmb.2008.04.011, 18455188.
29. Hagemeier SR, Dickerson SJ, Meng Q, Yu X, Mertz JE, Kenney SC. Sumoylation of the Epstein-Barr virus BZLF1 protein inhibits its transcriptional activity and is regulated by the virus-encoded protein kinase. J Virol 2010, 84:4383-4394. 10.1128/JVI.02369-09, 2863741, 20181712.
30. Wimmer P, Schreiner S, Dobner T. Human pathogens and the host cell SUMOylation system. J Virol 2012, 86:642-654. 10.1128/JVI.06227-11, 3255802, 22072786.
31. Wen KW, Damania B. Kaposi sarcoma-associated herpesvirus (KSHV): molecular biology and oncogenesis. Cancer Lett 2010, 289:140-150. 10.1016/j.canlet.2009.07.004, 19651473.
32. Moore PS, Chang Y. Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat Rev Cancer 2010, 10:878-889. 3718018, 21102637.
33. Chang Y, Moore PS. Kaposi's Sarcoma (KS)-associated herpesvirus and its role in KS. Infect Agents Dis 1996, 5:215-222.
34. Boshoff C, Schulz TF, Kennedy MM, Graham AK, Fisher C, Thomas A, McGee JO, Weiss RA, O'Leary JJ. Kaposi's sarcoma-associated herpesvirus infects endothelial and spindle cells. Nat Med 1995, 1:1274-1278. 10.1038/nm1295-1274, 7489408.
35. Coscoy L. Immune evasion by Kaposi's sarcoma-associated herpesvirus. Nat Rev Immunol 2007, 7:391-401. 10.1038/nri2076, 17457345.
36. Lee HR, Brulois K, Wong L, Jung JU. Modulation of immune system by Kaposi's sarcoma-associated herpesvirus: lessons from viral evasion strategies. Front Microbiol 2012, 3:44. 3293256, 22403573.
37. Lefort S, Soucy-Faulkner A, Grandvaux N, Flamand L. Binding of Kaposi's sarcoma-associated herpesvirus K-bZIP to interferon-responsive factor 3 elements modulates antiviral gene expression. J Virol 2007, 81:10950-10960. 10.1128/JVI.00183-07, 2045525, 17652396.
38. Yu Y, Wang SE, Hayward GS. The KSHV immediate-early transcription factor RTA encodes ubiquitin E3 ligase activity that targets IRF7 for proteosome-mediated degradation. Immunity 2005, 22:59-70. 10.1016/j.immuni.2004.11.011, 15664159.
39. Lefort S, Gravel A, Flamand L. Repression of interferon-alpha stimulated genes expression by Kaposi's sarcoma-associated herpesvirus K-bZIP protein. Virology 2010, 408:14-30. 10.1016/j.virol.2010.07.027, 20870261.
40. Bentz GL, Shackelford J, Pagano JS. Epstein-Barr virus latent membrane protein 1 regulates the function of interferon regulatory factor 7 by inducing its sumoylation. J Virol 2012, 86:12251-12261. 10.1128/JVI.01407-12, 3486478, 22951831.
41. Kubota T, Matsuoka M, Chang TH, Tailor P, Sasaki T, Tashiro M, Kato A, Ozato K. Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J Biol Chem 2008, 283:25660-25670. 10.1074/jbc.M804479200, 2533075, 18635538.
42. Richner JM, Clyde K, Pezda AC, Cheng BY, Wang T, Kumar GR, Covarrubias S, Coscoy L, Glaunsinger B. Global mRNA degradation during lytic gammaherpesvirus infection contributes to establishment of viral latency. PLoS Pathog 2011, 7:e1002150. 10.1371/journal.ppat.1002150, 3141057, 21811408.
43. Smiley JR. Herpes simplex virus virion host shutoff protein: immune evasion mediated by a viral RNase?. J Virol 2004, 78:1063-1068. 10.1128/JVI.78.3.1063-1068.2004, 321390, 14722261.
44. Covarrubias S, Gaglia MM, Kumar GR, Wong W, Jackson AO, Glaunsinger BA. Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. PLoS Pathog 2011, 7:e1002339. 10.1371/journal.ppat.1002339, 3203186, 22046136.
45. Chang PC, Fitzgerald LD, Hsia DA, Izumiya Y, Wu CY, Hsieh WP, Lin SF, Campbell M, Lam KS, Luciw PA, et al. Histone demethylase JMJD2A regulates Kaposi's sarcoma-associated herpesvirus replication and is targeted by a viral transcriptional factor. J Virol 2011, 85:3283-3293. 10.1128/JVI.02485-10, 3067885, 21228229.
46. Liu HW, Zhang J, Heine GF, Arora M, Gulcin Ozer H, Onti-Srinivasan R, Huang K, Parvin JD. Chromatin modification by SUMO-1 stimulates the promoters of translation machinery genes. Nucleic Acids Res 2012, 40:10172-10186. 10.1093/nar/gks819, 3488252, 22941651.
47. Chang CC, Naik MT, Huang YS, Jeng JC, Liao PH, Kuo HY, Ho CC, Hsieh YL, Lin CH, Huang NJ, et al. Structural and functional roles of Daxx SIM phosphorylation in SUMO paralog-selective binding and apoptosis modulation. Mol Cell 2011, 42:62-74. 10.1016/j.molcel.2011.02.022, 21474068.
48. Lyst MJ, Stancheva I. A role for SUMO modification in transcriptional repression and activation. Biochem Soc Trans 2007, 35:1389-1392. 10.1042/BST0351389, 2871292, 18031228.
49. Davies L, Gather U. The identification of multiple outliers. J Am Stat Assoc 1993, 88:782-792.
50. 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. 10.1016/j.molcel.2007.12.032, 18374648.
51. Zhang XD, Goeres J, Zhang H, Yen TJ, Porter AC, Matunis MJ. SUMO-2/3 modification and binding regulate the association of CENP-E with kinetochores and progression through mitosis. Mol Cell 2008, 29:729-741. 10.1016/j.molcel.2008.01.013, 2366111, 18374647.
52. Liang Q, Deng H, Li X, Wu X, Tang Q, Chang TH, Peng H, Rauscher FJ, Ozato K, Zhu F. Tripartite motif-containing protein 28 is a small ubiquitin-related modifier E3 ligase and negative regulator of IFN regulatory factor 7. J Immunol 2011, 187:4754-4763. 10.4049/jimmunol.1101704, 3197880, 21940674.
53. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, Epstein CB, Frietze S, Harrow J, Kaul R, et al. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. 10.1038/nature11247, 3439153, 22955616.
54. Cheng CY, Chu CH, Hsu HW, Hsu FR, Tang CY, Wang WC, Kung HJ, Chang PC. An improved ChIP-seq peak detection system for simultaneously identifying post-translational modified transcription factors by combinatorial fusion, using SUMOylation as an example. APBC2014 (Accepted).
55. Marusic MB, Mencin N, Licen M, Banks L, Grm HS. Modification of human papillomavirus minor capsid protein L2 by sumoylation. J Virol 2010, 84:11585-11589. 10.1128/JVI.01269-10, 2953202, 20739540.